- Email: [email protected]
Meningococcal vaccination for international travellers from Greece visiting developing countries
+
MODEL
Travel Medicine and Infectious Disease (2016) xx, 1e6
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.elsevierhealth.com/journals/tmid
Meningococcal vaccination for international travellers from Greece visiting developing countries Androula Pavli a, Panagiotis Katerelos b, Paraskevi Smeti a, Helena C. Maltezou b,* a
Travel Medicine Office, Hellenic Center for Disease Control and Prevention, Athens, Greece Department for Interventions in Health Care Facilities, Hellenic Center for Disease Control and Prevention, Athens, Greece
b
Received 11 September 2014; received in revised form 10 February 2016; accepted 1 March 2016
KEYWORDS Pre-travel; Meningitis; Vaccination; Travellers
Summary Background: Meningococcal meningitis is a serious disease. Travel-associated infection for the general traveller is low; however regular epidemics in indigenous population, particularly in sub-Saharan Africa are responsible for significant morbidity and mortality. Our aim was to assess meningococcal vaccination for international travellers from Greece. Methods: A prospective questionnaire-based study was conducted during 2009e2013. Results: A total of 5283 travellers were studied (median age: 39.2 years); Meningococcal tetravalent vaccine (A,C,W135,Y) was delivered to 1150 (21.8%) of them. Of those who travelled to the Middle East and sub-Saharan Africa, 73.1% and 21.2% received meningococcal vaccine, respectively. Of those travellers who travelled to sub-Saharan Africa from November to June and from July to October, 22.1% and 20.6% were vaccinated with meningococcal vaccine, respectively. Of all travellers who travelled for <1 month and 1 month, 23.3%, and 20.5%, were vaccinated, respectively. Meningococcal vaccine was administered to 95.3% of pilgrims, 17.4% of those visiting friends and relatives (VFRs), 16.7% of those who travelled for recreation, and 13.8% of those who travelled for work. Of travellers who stayed in urban, in rural, and in urban and rural areas, 32%, 11.6% and 12.7% were vaccinated, respectively. Meningococcal vaccine was delivered to 29.2%, 21.1%, 19.4% and 5.1% of those who stayed in hotels, at local people’s home, in camps, and on ships, respectively. The association of meningococcal vaccine administration with the destination, duration and purpose of travel, area of stay and type of accommodation was statistically significant. Conclusion: There is a need to improve meningococcal vaccine recommendations for travellers
* Corresponding author. Department for Interventions in Health-Care Facilities, Hellenic Center for Disease Control and Prevention, 3-5 Agrafon Street, Athens 15123, Greece. Tel.: þ30 210 5212 175. E-mail address: [email protected] (H.C. Maltezou). http://dx.doi.org/10.1016/j.tmaid.2016.03.001 1477-8939/ª 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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MODEL
2
A. Pavli et al. from Greece, particularly for high risk populations, such as VFRs, business travellers and those visiting sub-Saharan Africa especially during the dry season. ª 2016 Elsevier Ltd. All rights reserved.
1. Introduction
2. Methods
Neisseria meningitidis, a gram-negative diplococcal bacterium is recognized as the cause of meningococcal disease and a significant public health problem. Neisseria species which usually reside in the nasopharynx of asymptomatic people (4e35% of healthy adults) are easily transmitted to close contacts by respiratory droplets [1]. The incidence of invasive meningococcal disease varies both geographically and with time and in both endemic and epidemic forms is responsible for significant morbidity and mortality worldwide with 5e10% fatality rate [1,2]. Approximately 10e20% of survivors are left with permanent neurological sequelae despite all advances in therapy [1,2]. Meningococcal meningitis epidemics affect more than 400 million people living in the African “meningitis belt” (from Senegal to Ethiopia) annually and during epidemics as many as 1000/100,000 population may be affected [2]. Serogroup A and, less frequently serogroup C, have been responsible for epidemics in the past in Africa and recently, firstly in Saudi Arabia, and later in West Africa, W135 has emerged as a serogroup. Serogroups X and Y are rare, but associated with slowly increasing trends [1]. The risk of acquiring meningococcal disease in general depends on the region, the living conditions and behaviour [1]. International travel and migration may contribute to the importation and rapid spread of meningococcal disease; Africa has been one of the fastest-growing touristic regions of the last decade with 6% more international tourist arrivals recorded in 2013 compared to previous years, equivalent to an increase of three million tourists [3]. The incidence of meningococcal disease in international travellers is low; it is estimated to be 0.4/100,000 travellers/month [4,5]. Risk factors for the acquisition of the disease include destination, duration and season of travel and living in close contact with the local people [6]. Mass gatherings such as the Hajj pilgrimage to Saudi Arabia have been associated with outbreaks of meningococcal disease and it is considered a risk factor [7]. The serogroup A and W135 were responsible for the outbreaks in 1998 and in the years 2000 and 2001, respectively [8]. Vaccination against meningococcal disease is required for Hajj/Umrah pilgrims to Saudi Arabia. Tetravalent polysaccharide and conjugate meningococcal vaccines (A, C, W-135 and Y) are recommended for travellers’ to African “meningitis belt”. The new conjugate vaccines may help protect travellers and decrease the spread of bacterial carriage and disease [9,10]. The current study was conducted by the Hellenic Center for Disease Control and Prevention in order to evaluate the application of meningococcal vaccine recommendations for international travellers.
In Greece travel medical services are provided predominantly by the 57 Public Health Departments across the country. Travel health providers include physicians, nurses and health visitors specialized in public health. Pre-travel consultation services are provided in accordance with the national guidelines which are similar to World Health Organization, and the Centers for Disease Control and Prevention guidelines [5,11,12]. The meningococcal polysaccharide vaccine is available exclusively in the Public Health Departments. The conjugated (with CRM 197) tetravalent (A,C,W135,Y) meningococcal vaccine has been available on the Greek market since 2011 and it is fully reimbursed for individuals over 11 years of age; this vaccine can be administered by other primary care practitioners as well. Other conjugated (with tetanus toxoid or diphtheria toxoid) tetravalent meningococcal vaccines have not yet been available. All international travellers who attended all 57 Public Health Departments for pre-travel advice from 1 January, 2009 through December 31, 2013, were asked to participate in a questionnaire-based study. Consent was requested from all participants. The questionnaire (anonymous form) was developed by the researchers and included the following data which were collected prospectively per traveller: age, gender, date of departure, country of destination, duration of stay, type and purpose of travel, visiting areas, type of accommodation, participation in outdoor activities, vaccination and malaria prophylaxis recommendations. Urban accommodation was defined as cities with population of 5000 people, whereas rural accommodation was defined as villages of <5000 population or staying in the countryside. Short-term and long-term travel was defined as a trip of <1 month duration and 1 month, respectively. Statistical analysis was performed using the STATA 8.0 statistical package. The multivariable logistic regression was applied to investigate the relation between prescription of meningococcal vaccine and travellers’ and travel characteristics. c2 test was used in each one of the destination areas separately in order to investigate the relation between meningococcal vaccine administration and duration of travel in each destination area. p-Values of 0.05 or less were considered statistically significant.
3. Results During the study period 5283 travellers were studied. The participation rate ranged from 75% to 85% per Health Department. Most participants (40%) were seen in the
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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Meningococcal vaccination for travellers from Greece Table 1
3
Meningococcal vaccine administration rates among international travellers from Greece by travel destination.
Regiona (p-value < 0.001)
Vaccinated travellers (%)
Non-vaccinated travellers (%)
Total travellers
Sub-Saharan Africa North Africa South Africa Indian subcontinent Southeast Asia East Asia Middle East South America Central America Caribbean Europe North America Australia/Oceania
488 9 31 45 19 6 517 28 0 1 3 1 2
1812 104 181 412 302 178 190 699 44 20 99 79 13
2300 113 212 457 321 184 707 727 44 21 102 80 15
a
(21.2) (8.0) (14.6) (9.8) (5.9) (3.3) (73.1) (3.9) (0.0) (4.8) (2.9) (1.3) (13.3)
(78.8) (92) (85.4) (90.2) (94.1) (96.7) (26.9) (96.1) (100) (95.2) (97.1) (98.7) (86.7)
The regions are classified according to United Nations Statistics Division [26].
prefecture of Attica, where one third of the Greek population resides. International travellers sought pre-travel advice at a median of 15 days (range: 0e349 days) before their departure. Median age of the study group was 39.2 years and 64.3% of them were male. The majority of the travellers were Greek nationals (96.4%). Meningococcal vaccine was delivered to 1150 (21.8%) of them; 45%, 42.4%, 3.9% and 2.7% of them travelled to the Middle East, subSaharan Africa, the Indian subcontinent and South Africa, respectively. Pilgrims accounted for 83% (430) of all travellers to the Middle East. Sub-Saharan Africa was the most common destination (43.5%) followed by South America (13.8%), the Middle East (13.4%), the Indian subcontinent (8.7%), Southeast Asia (6.1%), South Africa (4%) and East Asia (3.5%) among all
Table 2
travellers of the study group. Of those who travelled to the Middle East, sub-Saharan Africa, and South Africa 73.1%, 21.2% and 14.6% received meningococcal vaccine, respectively (Table 1). Table 2 describes meningococcal vaccination according to travel characteristics. Regarding duration of travel, 2972 (56.3%) stayed <1 month and 2083 (39.3%) 1 month; 23.3% and 20.5% received meningococcal vaccination, respectively. In terms of purpose of travel 2041 (38.6%) travelled for recreation, 2271 (43%) for work, 430 (8.1%) for religious reasons and 224 (4.2%) for visiting friends and relatives (VFRs); meningococcal vaccination was administered to 16.7%, 13.8%, 95.3% and 17.4% of them, respectively. According to the type of accommodation, 768 (14.5%) stayed at local people’s home; Meningococcal vaccine was
Meningococcal vaccine administration according to travel characteristics (N Z 5238). Vaccinated travellers (%)
Non-vaccinated travellers (%)
Total travellers
Purpose of travel Recreation Business Religious reasons VFRsa
341 314 410 39
1700 1957 20 185
(83.3) (86.2) (4.7) (82.6)
2041 2271 430 224
Duration of travel <1 month 1 month
692 (23.3) 427 (20.5)
2280 (76.7) 1656 (79.5)
2972 2083
Type of accommodation Hotel Local people’s home Camp Shipb
886 162 18 60
2153 606 75 1119
(70.8) (78.9) (80.6) (94.9)
3039 768 93 1179
Area of stay Urban Rural Urban & rural
938 (32.0) 14 (11.6) 44 (12.7)
1995 (68) 107 (88.4) 1089 (87.3)
2933 121 1133
a b
p-Value < 0.001 (16.7) (13.8) (95.3) (17.4)
p-Value < 0.001
p-Value Z 0.002 (29.2) (21.1) (19.4) (5.1)
p-Value < 0.001
Visiting friends and relatives. Travellers were sailors.
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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A. Pavli et al. Table 3 Meningococcal vaccine administration rates among international travellers from Greece to sub-Saharan Africa according to travel characteristics. Destination
Vaccinated travellers
Non-vaccinated travellers
Total travellers
Sub Saharan Africa
N Z 488 (%)
N Z 1812 (%)
N Z 2300
Duration <1 month 1 month
309 (20.4) 160 (24.1)
1204 (79.6) 503 (75.9)
1513 663
Season NovembereJune JulyeOctober
306 (22.1) 159 (20.6)
1077 (77.9) 612 (79.4)
1383 771
Purpose Recreation Business VFRs
196 (21.2) 228 (21.1) 26 (19.1)
729 (78.8) 851 (78.9)
925 1079 136
Place of stay Urban Rural Urban and rural
336 (25.2) 11 (17.2) 111 (20.4)
997 (74.8) 53 (82.8) 433 (79.6)
1333 64 544
Accommodation Hotel House Shipa Camping
319 (23.8) 111 (23.3) 33 (10) 14 (29.8)
1024 (76.2) 366 (76.7) 298 (90) 33 (70.2)
1343 477 331 47
a
p-Value
<0.001
e
e
e
e
Travellers were sailors.
administered 21.1% (Table 2). Outdoor activities were reported by 699 (13.2%) of all travellers; 13% of those were vaccinated. Meningococcal vaccination rates for travellers to subSaharan Africa according to travel characteristics are shown in Table 3; 336 (22.1%) of the travellers who visited sub-Saharan Africa from November to June, 160 (24.1%) of the travellers who stayed for 1 month and 111 (23.3%) of those who stayed with indigenous population were administered meningococcal vaccination, respectively. In logistic regression analysis, the association of meningococcal vaccine administration was statistically significant with the destination area, duration and purpose of travel, area of stay (p-value < 0.001) and type of accommodation (p-value Z 0.002). For sub-Saharan Africa, statistically significant was found the association of meningococcal vaccination with duration of travel (p-value < 0.001) (Table 3).
4. Discussion Meningococcal disease is a rare disease in travellers; however the complications of this infection are very serious and can be devastating for any person. Thus, it is crucial when assessing travellers for vaccination, to consider not only the incidence and the associated fatality rates but also the long-term consequences of the infection [13,14]. Factors to consider when making a decision about vaccination include destination such as the sub-Saharan Africa [15], in particular during the dry season from November to June, travel for long period of time, staying with the indigenous
population, and working at the destination and sharing crowded accommodation or transportation [6,14]. In addition meningococcal vaccination should be advised to travellers visiting areas with current outbreaks and epidemics [6,14] and to those who may be exposed to sporadic cases of meningococcal disease such as areas where young adults and adolescents congregate (e.g. schools, college dormitories). People with immunodeficiencies, splenectomy or complement deficiencies should receive the meningococcus vaccine regardless of travel destination [6,14]. Taking in account the large variety of geographical distribution worldwide, broad coverage against all vaccine-preventable serogroups is recommended with multivalent and in particular conjugate meningococcal vaccines which are beneficial considering that the aim of immunization is to reduce the risk of the disease in travellers as well as to reduce the spread to others [6,14]. Prior to 2002, outbreaks of meningococcal disease were reported among Hajj pilgrims, their contacts, and thereafter even in persons without a history of contact. This prompted the authorities of the Kingdom of Saudi Arabia to issue a quadrivalent meningococcal vaccination requirement to obtain a Hajj visa [16]. In the current study 95.3% of all pilgrims to Saudi Arabia received meningococcal vaccination and the remaining 4.7% had an appropriate history of immunization in the past. Our results showed statistically significant association between destination and meningococcal vaccination. However, meningococcal vaccination rate of travellers to high risk destinations [16] such as the sub-Saharan Africa (21.8%) was lower than expected, comparable to that of
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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Meningococcal vaccination for travellers from Greece another recent Greek study (26.6%) [17] and higher compared to the results of a Sao Paulo University study (3.8%) [18]. Although duration of travel appears to be associated with diseases transmitted through contact with people [19], meningococcal vaccination rate of long-term travellers in the current study was lower than expected. More than one third of the study group travelled for 1 month and only 20.5% of them received meningococcal vaccination and 24.1% of those who travelled to sub-Saharan Africa. Expatriates including business travellers are a distinct population at unique risk for health problems related to their travel exposure [20]. In our study, business travellers accounted for 48% of all travellers; only 21.1% of those travelling to sub-Saharan Africa received meningococcal vaccination. Vaccine recommendations for business travellers need to focus on destination, activities and underlying health conditions, taking into consideration the concept of cumulative risk for frequent or long term travel [21]. Low vaccination rate may be related to poor perception of business travellers about health prevention as shown by previous studies [22,23]. In our study 17.4% of all travellers VFRs and 19.1% of those visiting the sub-Saharan Africa received meningococcal vaccine. Travellers VFRs represent a major group at risk for imported diseases to industrialized countries [21]. While staying in close contact with relatives or friends, and for longer period of time [24,25], VFRs may be at higher risk for the acquisition of meningococcal infection, especially those going to sub-Saharan Africa [6]. The low vaccination coverage probably indicates a lack of pre-travel advice and opportunity to provide preventative vaccination [24,25]. Close contact with people such as staying in local people’s home also represents a risk for acquisition of meningococcal disease [6,14], however meningococcal vaccine administration was lower than expected; only 23.3% of travellers who planned to stay with indigenous people in sub-Saharan Africa received vaccination. Retrospective analysis of data showed that all travellers with immunodeficiency were administered meningococcal vaccination. Meningococcal vaccine recommendations for high risk groups such as long-term travellers, business travellers and VFRs were below expectations. However for pilgrims for whom the meningococcal vaccine (A < C < W135,Y) is required the vaccination rate was appropriate. Meningococcal vaccination recommendations therefore should be improved. A clear strength of our cohort is the prospective study of a large number of international travellers which gave us the opportunity to study a wide range of travellers’ characteristics and meningococcal vaccine recommendations. The fact that we have no data regarding those who refused vaccination and those who received vaccination (after 2011) by other health providers is a limitation. There is a need to increase awareness of travel health consultants about meningococcal vaccination recommendations in travellers which should be more selective and individualized and based on careful assessment of the known risk factors for disease acquisition. Furthermore Public Health Authorities should develop strategies in order educate high risk populations such as VFRs and business travellers about risks and prophylaxis. The aim of
5 vaccinating travellers is to both protect the individual from meningococcal disease and protect others from its transmission as well as to prevent the international spread of infection.
Conflict of interest There is no conflict of interest to declare.
References [1] World Health Organization. Wkly Epidemiol Rec 2011;86: 521e39. [2] Jafri RZ, Ali A, Messonnier NE, Tevi-Benissan C, Durrheim D, Eskola J, et al. Global epidemiology of invasive meningococcal disease. Popul Health Metr 2013;11:17. [3] World Tourism Organization. Available at: http:// dtxtq4w60xqpw.cloudfront.net/sites/all/files/pdf/unwto_ highlights13_en_hr.pdf [accessed 20.05.14]. [4] Wilder-Smith A. Meningococcal vaccine in travellers. Curr Opin Infect Dis 2007;20(5):454e60. [5] Koch S, Steffen R. Meningococcal disease in travellers: vaccination recommendations. J Travel Med 1994;1(1):4e7. [6] World Health Organization International Travel and Health. Available at: http://www.who.int/ith/ITH_chapter_6.pdf? uaZ1 [accessed 20.05.14]. [7] Wilder-Smith A, Memish Z. Meningococcal disease and travel. Int J Antimicrob Agents 2003;21(2):102e6. [8] Wilder-Smith A, Goh KT, Barkham T, Paton NI. Hajj-associated outbreak strain of Neisseria meningitidis serogroup W135: estimates of the attack rate in a defined population and the risk of invasive disease developing in carriers. Clin Infect Dis 2003;36(6):679e83. [9] Wilder-Smith A. Meningococcal disease: risk for international travellers and vaccine strategies. Travel Med Infect Dis 2008; 6:182e6. [10] Cramer JP, Wilder-Smith A. Meningococcal disease in travellers: update on vaccine options. Curr Opin Infect Dis 2012;25: 507e17. [11] Hellenic Centre for Disease Control and Prevention. Available at: http://www.keelpno.gr/el gr/taxidiutikήiatri kή/katεyqyntήriε2odhgίε2taxidiutikή2iatrikή2/εmbόlia [accessed 21.05.14]. [12] Centers for Disease Control and Prevention. Available at: http://wwwnc.cdc.gov/travel/ [accessed 21.05.14]. [13] Steffen R, Connor BA. Vaccines in travel health: from risk assessment to priorities. J Travel Med 2005;12:26e35. [14] Steffen R. The risk of meningococcal disease in travellers and current recommendations for prevention. J Travel Med 2010; 17(Suppl):9e17. [15] Parent du Chatelet I, Barboza P, Taha MK. W135 invasive meningococcal infections imported from Sub-Saharan Africa to France, January to April 2012. Euro Surveill 2012 May 24;17. [16] Ministry of Hajj. Kingdom of Saudi Arabia. Important notices. Visas. Available at: http://www.haj.gov.sa/en-us/SitePages/ News-View.aspx [accessed 22.05.14]. [17] Pavli A, Spilioti A, Smeti P, Patrinos S, Maltezou HC. Vaccination and malaria prevention among international travellers departing from Athens International Airport to African destinations. J Trop Med 2014;2014:563030. http: //dx.doi.org/10.1155/2014/563030 [Epub 2014 Mar 2]. [18] Chinwa Lo S, Mascheretti M, Chaves Tdo S, Lopes MH. Travellers’ vaccinations: experience from the Travellers’ Clinic of Hospital das Clı´nicas, University of Sa ˜o Paulo School of Medicine. Rev Soc Bras Med Trop 2008;41:474e8.
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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6 [19] Chen LH, Wilson ME, Davis X, Loutan L, Schwartz E, Keystone J, et al. Illness in long-term travellers visiting GeoSentinel clinics. Emerg Infect Dis 2009;15:1773e82. [20] Lim PL, Han P, Chen LH, MacDonald S, Pandey P, Hale D, et al. Expatriates ill after travel: results from the geosentinel surveillance network. BMC Infect Dis 2012;12:386. http: //dx.doi.org/10.1186/1471-2334-12-386. [21] Gautret P, Schlagenhauf P, Gaudart J, Castelli F, Brouqui P, von Sonnenburg F, et al. Multicenter EuroTravNet/GeoSentinel study of travel-related infectious diseases in Europe. Emerg Infect Dis 2009 Nov;15:1783e90. http: //dx.doi.org/10.3201/eid1511.091147. [22] Pavli A, Silvestros C, Patrinos S, Lymperi I, Maltezou HC. Pretravel preparation practices among business travellers to tropical and subtropical destinations: results from the Athens International Airport Survey. Travel Med Infect Dis 2013 Dec
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24. http://dx.doi.org/10.1016/j.tmaid.2013.12.004. pii: S1477-8939(13)00218-4 [Epub ahead of print]. Wynberg E, Toner S, Wendt JK, Visser LG, Breederveld D, Berg J. Business travellers’ risk perception of infectious diseases: where are the knowledge gaps, and how serious are they? J Travel Med 2013;20:11e6. Angell SY, Behrens RH. Risk assessment and disease prevention in travellers visiting friends and relatives. Infect Dis Clin North Am 2005;19:49e65. Angell SY, Cetron MS. Health disparities among travellers visiting friends and relatives abroad. Ann Int Med 2005;142: 67e73. United Nations Statistics Division. Available at: http:// unstats.un.org/unsd/methods/m49/m49regin.htm [accessed 03.02.16].
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
MODEL
Travel Medicine and Infectious Disease (2016) xx, 1e6
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.elsevierhealth.com/journals/tmid
Meningococcal vaccination for international travellers from Greece visiting developing countries Androula Pavli a, Panagiotis Katerelos b, Paraskevi Smeti a, Helena C. Maltezou b,* a
Travel Medicine Office, Hellenic Center for Disease Control and Prevention, Athens, Greece Department for Interventions in Health Care Facilities, Hellenic Center for Disease Control and Prevention, Athens, Greece
b
Received 11 September 2014; received in revised form 10 February 2016; accepted 1 March 2016
KEYWORDS Pre-travel; Meningitis; Vaccination; Travellers
Summary Background: Meningococcal meningitis is a serious disease. Travel-associated infection for the general traveller is low; however regular epidemics in indigenous population, particularly in sub-Saharan Africa are responsible for significant morbidity and mortality. Our aim was to assess meningococcal vaccination for international travellers from Greece. Methods: A prospective questionnaire-based study was conducted during 2009e2013. Results: A total of 5283 travellers were studied (median age: 39.2 years); Meningococcal tetravalent vaccine (A,C,W135,Y) was delivered to 1150 (21.8%) of them. Of those who travelled to the Middle East and sub-Saharan Africa, 73.1% and 21.2% received meningococcal vaccine, respectively. Of those travellers who travelled to sub-Saharan Africa from November to June and from July to October, 22.1% and 20.6% were vaccinated with meningococcal vaccine, respectively. Of all travellers who travelled for <1 month and 1 month, 23.3%, and 20.5%, were vaccinated, respectively. Meningococcal vaccine was administered to 95.3% of pilgrims, 17.4% of those visiting friends and relatives (VFRs), 16.7% of those who travelled for recreation, and 13.8% of those who travelled for work. Of travellers who stayed in urban, in rural, and in urban and rural areas, 32%, 11.6% and 12.7% were vaccinated, respectively. Meningococcal vaccine was delivered to 29.2%, 21.1%, 19.4% and 5.1% of those who stayed in hotels, at local people’s home, in camps, and on ships, respectively. The association of meningococcal vaccine administration with the destination, duration and purpose of travel, area of stay and type of accommodation was statistically significant. Conclusion: There is a need to improve meningococcal vaccine recommendations for travellers
* Corresponding author. Department for Interventions in Health-Care Facilities, Hellenic Center for Disease Control and Prevention, 3-5 Agrafon Street, Athens 15123, Greece. Tel.: þ30 210 5212 175. E-mail address: [email protected] (H.C. Maltezou). http://dx.doi.org/10.1016/j.tmaid.2016.03.001 1477-8939/ª 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
+
MODEL
2
A. Pavli et al. from Greece, particularly for high risk populations, such as VFRs, business travellers and those visiting sub-Saharan Africa especially during the dry season. ª 2016 Elsevier Ltd. All rights reserved.
1. Introduction
2. Methods
Neisseria meningitidis, a gram-negative diplococcal bacterium is recognized as the cause of meningococcal disease and a significant public health problem. Neisseria species which usually reside in the nasopharynx of asymptomatic people (4e35% of healthy adults) are easily transmitted to close contacts by respiratory droplets [1]. The incidence of invasive meningococcal disease varies both geographically and with time and in both endemic and epidemic forms is responsible for significant morbidity and mortality worldwide with 5e10% fatality rate [1,2]. Approximately 10e20% of survivors are left with permanent neurological sequelae despite all advances in therapy [1,2]. Meningococcal meningitis epidemics affect more than 400 million people living in the African “meningitis belt” (from Senegal to Ethiopia) annually and during epidemics as many as 1000/100,000 population may be affected [2]. Serogroup A and, less frequently serogroup C, have been responsible for epidemics in the past in Africa and recently, firstly in Saudi Arabia, and later in West Africa, W135 has emerged as a serogroup. Serogroups X and Y are rare, but associated with slowly increasing trends [1]. The risk of acquiring meningococcal disease in general depends on the region, the living conditions and behaviour [1]. International travel and migration may contribute to the importation and rapid spread of meningococcal disease; Africa has been one of the fastest-growing touristic regions of the last decade with 6% more international tourist arrivals recorded in 2013 compared to previous years, equivalent to an increase of three million tourists [3]. The incidence of meningococcal disease in international travellers is low; it is estimated to be 0.4/100,000 travellers/month [4,5]. Risk factors for the acquisition of the disease include destination, duration and season of travel and living in close contact with the local people [6]. Mass gatherings such as the Hajj pilgrimage to Saudi Arabia have been associated with outbreaks of meningococcal disease and it is considered a risk factor [7]. The serogroup A and W135 were responsible for the outbreaks in 1998 and in the years 2000 and 2001, respectively [8]. Vaccination against meningococcal disease is required for Hajj/Umrah pilgrims to Saudi Arabia. Tetravalent polysaccharide and conjugate meningococcal vaccines (A, C, W-135 and Y) are recommended for travellers’ to African “meningitis belt”. The new conjugate vaccines may help protect travellers and decrease the spread of bacterial carriage and disease [9,10]. The current study was conducted by the Hellenic Center for Disease Control and Prevention in order to evaluate the application of meningococcal vaccine recommendations for international travellers.
In Greece travel medical services are provided predominantly by the 57 Public Health Departments across the country. Travel health providers include physicians, nurses and health visitors specialized in public health. Pre-travel consultation services are provided in accordance with the national guidelines which are similar to World Health Organization, and the Centers for Disease Control and Prevention guidelines [5,11,12]. The meningococcal polysaccharide vaccine is available exclusively in the Public Health Departments. The conjugated (with CRM 197) tetravalent (A,C,W135,Y) meningococcal vaccine has been available on the Greek market since 2011 and it is fully reimbursed for individuals over 11 years of age; this vaccine can be administered by other primary care practitioners as well. Other conjugated (with tetanus toxoid or diphtheria toxoid) tetravalent meningococcal vaccines have not yet been available. All international travellers who attended all 57 Public Health Departments for pre-travel advice from 1 January, 2009 through December 31, 2013, were asked to participate in a questionnaire-based study. Consent was requested from all participants. The questionnaire (anonymous form) was developed by the researchers and included the following data which were collected prospectively per traveller: age, gender, date of departure, country of destination, duration of stay, type and purpose of travel, visiting areas, type of accommodation, participation in outdoor activities, vaccination and malaria prophylaxis recommendations. Urban accommodation was defined as cities with population of 5000 people, whereas rural accommodation was defined as villages of <5000 population or staying in the countryside. Short-term and long-term travel was defined as a trip of <1 month duration and 1 month, respectively. Statistical analysis was performed using the STATA 8.0 statistical package. The multivariable logistic regression was applied to investigate the relation between prescription of meningococcal vaccine and travellers’ and travel characteristics. c2 test was used in each one of the destination areas separately in order to investigate the relation between meningococcal vaccine administration and duration of travel in each destination area. p-Values of 0.05 or less were considered statistically significant.
3. Results During the study period 5283 travellers were studied. The participation rate ranged from 75% to 85% per Health Department. Most participants (40%) were seen in the
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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Meningococcal vaccination for travellers from Greece Table 1
3
Meningococcal vaccine administration rates among international travellers from Greece by travel destination.
Regiona (p-value < 0.001)
Vaccinated travellers (%)
Non-vaccinated travellers (%)
Total travellers
Sub-Saharan Africa North Africa South Africa Indian subcontinent Southeast Asia East Asia Middle East South America Central America Caribbean Europe North America Australia/Oceania
488 9 31 45 19 6 517 28 0 1 3 1 2
1812 104 181 412 302 178 190 699 44 20 99 79 13
2300 113 212 457 321 184 707 727 44 21 102 80 15
a
(21.2) (8.0) (14.6) (9.8) (5.9) (3.3) (73.1) (3.9) (0.0) (4.8) (2.9) (1.3) (13.3)
(78.8) (92) (85.4) (90.2) (94.1) (96.7) (26.9) (96.1) (100) (95.2) (97.1) (98.7) (86.7)
The regions are classified according to United Nations Statistics Division [26].
prefecture of Attica, where one third of the Greek population resides. International travellers sought pre-travel advice at a median of 15 days (range: 0e349 days) before their departure. Median age of the study group was 39.2 years and 64.3% of them were male. The majority of the travellers were Greek nationals (96.4%). Meningococcal vaccine was delivered to 1150 (21.8%) of them; 45%, 42.4%, 3.9% and 2.7% of them travelled to the Middle East, subSaharan Africa, the Indian subcontinent and South Africa, respectively. Pilgrims accounted for 83% (430) of all travellers to the Middle East. Sub-Saharan Africa was the most common destination (43.5%) followed by South America (13.8%), the Middle East (13.4%), the Indian subcontinent (8.7%), Southeast Asia (6.1%), South Africa (4%) and East Asia (3.5%) among all
Table 2
travellers of the study group. Of those who travelled to the Middle East, sub-Saharan Africa, and South Africa 73.1%, 21.2% and 14.6% received meningococcal vaccine, respectively (Table 1). Table 2 describes meningococcal vaccination according to travel characteristics. Regarding duration of travel, 2972 (56.3%) stayed <1 month and 2083 (39.3%) 1 month; 23.3% and 20.5% received meningococcal vaccination, respectively. In terms of purpose of travel 2041 (38.6%) travelled for recreation, 2271 (43%) for work, 430 (8.1%) for religious reasons and 224 (4.2%) for visiting friends and relatives (VFRs); meningococcal vaccination was administered to 16.7%, 13.8%, 95.3% and 17.4% of them, respectively. According to the type of accommodation, 768 (14.5%) stayed at local people’s home; Meningococcal vaccine was
Meningococcal vaccine administration according to travel characteristics (N Z 5238). Vaccinated travellers (%)
Non-vaccinated travellers (%)
Total travellers
Purpose of travel Recreation Business Religious reasons VFRsa
341 314 410 39
1700 1957 20 185
(83.3) (86.2) (4.7) (82.6)
2041 2271 430 224
Duration of travel <1 month 1 month
692 (23.3) 427 (20.5)
2280 (76.7) 1656 (79.5)
2972 2083
Type of accommodation Hotel Local people’s home Camp Shipb
886 162 18 60
2153 606 75 1119
(70.8) (78.9) (80.6) (94.9)
3039 768 93 1179
Area of stay Urban Rural Urban & rural
938 (32.0) 14 (11.6) 44 (12.7)
1995 (68) 107 (88.4) 1089 (87.3)
2933 121 1133
a b
p-Value < 0.001 (16.7) (13.8) (95.3) (17.4)
p-Value < 0.001
p-Value Z 0.002 (29.2) (21.1) (19.4) (5.1)
p-Value < 0.001
Visiting friends and relatives. Travellers were sailors.
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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4
A. Pavli et al. Table 3 Meningococcal vaccine administration rates among international travellers from Greece to sub-Saharan Africa according to travel characteristics. Destination
Vaccinated travellers
Non-vaccinated travellers
Total travellers
Sub Saharan Africa
N Z 488 (%)
N Z 1812 (%)
N Z 2300
Duration <1 month 1 month
309 (20.4) 160 (24.1)
1204 (79.6) 503 (75.9)
1513 663
Season NovembereJune JulyeOctober
306 (22.1) 159 (20.6)
1077 (77.9) 612 (79.4)
1383 771
Purpose Recreation Business VFRs
196 (21.2) 228 (21.1) 26 (19.1)
729 (78.8) 851 (78.9)
925 1079 136
Place of stay Urban Rural Urban and rural
336 (25.2) 11 (17.2) 111 (20.4)
997 (74.8) 53 (82.8) 433 (79.6)
1333 64 544
Accommodation Hotel House Shipa Camping
319 (23.8) 111 (23.3) 33 (10) 14 (29.8)
1024 (76.2) 366 (76.7) 298 (90) 33 (70.2)
1343 477 331 47
a
p-Value
<0.001
e
e
e
e
Travellers were sailors.
administered 21.1% (Table 2). Outdoor activities were reported by 699 (13.2%) of all travellers; 13% of those were vaccinated. Meningococcal vaccination rates for travellers to subSaharan Africa according to travel characteristics are shown in Table 3; 336 (22.1%) of the travellers who visited sub-Saharan Africa from November to June, 160 (24.1%) of the travellers who stayed for 1 month and 111 (23.3%) of those who stayed with indigenous population were administered meningococcal vaccination, respectively. In logistic regression analysis, the association of meningococcal vaccine administration was statistically significant with the destination area, duration and purpose of travel, area of stay (p-value < 0.001) and type of accommodation (p-value Z 0.002). For sub-Saharan Africa, statistically significant was found the association of meningococcal vaccination with duration of travel (p-value < 0.001) (Table 3).
4. Discussion Meningococcal disease is a rare disease in travellers; however the complications of this infection are very serious and can be devastating for any person. Thus, it is crucial when assessing travellers for vaccination, to consider not only the incidence and the associated fatality rates but also the long-term consequences of the infection [13,14]. Factors to consider when making a decision about vaccination include destination such as the sub-Saharan Africa [15], in particular during the dry season from November to June, travel for long period of time, staying with the indigenous
population, and working at the destination and sharing crowded accommodation or transportation [6,14]. In addition meningococcal vaccination should be advised to travellers visiting areas with current outbreaks and epidemics [6,14] and to those who may be exposed to sporadic cases of meningococcal disease such as areas where young adults and adolescents congregate (e.g. schools, college dormitories). People with immunodeficiencies, splenectomy or complement deficiencies should receive the meningococcus vaccine regardless of travel destination [6,14]. Taking in account the large variety of geographical distribution worldwide, broad coverage against all vaccine-preventable serogroups is recommended with multivalent and in particular conjugate meningococcal vaccines which are beneficial considering that the aim of immunization is to reduce the risk of the disease in travellers as well as to reduce the spread to others [6,14]. Prior to 2002, outbreaks of meningococcal disease were reported among Hajj pilgrims, their contacts, and thereafter even in persons without a history of contact. This prompted the authorities of the Kingdom of Saudi Arabia to issue a quadrivalent meningococcal vaccination requirement to obtain a Hajj visa [16]. In the current study 95.3% of all pilgrims to Saudi Arabia received meningococcal vaccination and the remaining 4.7% had an appropriate history of immunization in the past. Our results showed statistically significant association between destination and meningococcal vaccination. However, meningococcal vaccination rate of travellers to high risk destinations [16] such as the sub-Saharan Africa (21.8%) was lower than expected, comparable to that of
Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001
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Meningococcal vaccination for travellers from Greece another recent Greek study (26.6%) [17] and higher compared to the results of a Sao Paulo University study (3.8%) [18]. Although duration of travel appears to be associated with diseases transmitted through contact with people [19], meningococcal vaccination rate of long-term travellers in the current study was lower than expected. More than one third of the study group travelled for 1 month and only 20.5% of them received meningococcal vaccination and 24.1% of those who travelled to sub-Saharan Africa. Expatriates including business travellers are a distinct population at unique risk for health problems related to their travel exposure [20]. In our study, business travellers accounted for 48% of all travellers; only 21.1% of those travelling to sub-Saharan Africa received meningococcal vaccination. Vaccine recommendations for business travellers need to focus on destination, activities and underlying health conditions, taking into consideration the concept of cumulative risk for frequent or long term travel [21]. Low vaccination rate may be related to poor perception of business travellers about health prevention as shown by previous studies [22,23]. In our study 17.4% of all travellers VFRs and 19.1% of those visiting the sub-Saharan Africa received meningococcal vaccine. Travellers VFRs represent a major group at risk for imported diseases to industrialized countries [21]. While staying in close contact with relatives or friends, and for longer period of time [24,25], VFRs may be at higher risk for the acquisition of meningococcal infection, especially those going to sub-Saharan Africa [6]. The low vaccination coverage probably indicates a lack of pre-travel advice and opportunity to provide preventative vaccination [24,25]. Close contact with people such as staying in local people’s home also represents a risk for acquisition of meningococcal disease [6,14], however meningococcal vaccine administration was lower than expected; only 23.3% of travellers who planned to stay with indigenous people in sub-Saharan Africa received vaccination. Retrospective analysis of data showed that all travellers with immunodeficiency were administered meningococcal vaccination. Meningococcal vaccine recommendations for high risk groups such as long-term travellers, business travellers and VFRs were below expectations. However for pilgrims for whom the meningococcal vaccine (A < C < W135,Y) is required the vaccination rate was appropriate. Meningococcal vaccination recommendations therefore should be improved. A clear strength of our cohort is the prospective study of a large number of international travellers which gave us the opportunity to study a wide range of travellers’ characteristics and meningococcal vaccine recommendations. The fact that we have no data regarding those who refused vaccination and those who received vaccination (after 2011) by other health providers is a limitation. There is a need to increase awareness of travel health consultants about meningococcal vaccination recommendations in travellers which should be more selective and individualized and based on careful assessment of the known risk factors for disease acquisition. Furthermore Public Health Authorities should develop strategies in order educate high risk populations such as VFRs and business travellers about risks and prophylaxis. The aim of
5 vaccinating travellers is to both protect the individual from meningococcal disease and protect others from its transmission as well as to prevent the international spread of infection.
Conflict of interest There is no conflict of interest to declare.
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Please cite this article in press as: Pavli A, et al., Meningococcal vaccination for international travellers from Greece visiting developing countries, Travel Medicine and Infectious Disease (2016), http://dx.doi.org/10.1016/j.tmaid.2016.03.001