Background The National Travel Health Network and Centre (NaTHNaC) introduced a program of registration, training, standards, and audit for yellow fever vaccination centers (YFVCs) in England, Wales, and Northern Ireland (EWNI) in 2005. Prior to rolling out the program, NaTHNaC surveyed YFVCs in England.
Objectives. To reassess the practice of YFVCs in 2009, 4 years after the institution of the NaTHNaC program, to identify areas for ongoing support, and to assess the impact of the program.
Methods In 2009, all YFVCs in EWNI were asked to complete a questionnaire on type of practice, administration of travel vaccines, staff training, vaccine storage and patient record keeping, use of travel health information, evaluation of NaTHNaC yellow fever (YF) training, and resource and training needs. Data were analyzed using Microsoft Excel® and STATA 9®.
Results The questionnaire was completed by 1,438 YFVCs (41.5% of 3,465 YFVCs). Most YFVCs were based in General Practice (87.4%). In nearly all YFVCs (97.0%), nurses advised travelers and administered YF vaccine. An annual median of 50 doses of YF vaccine was given by each YFVC. A total of 96.7% of nurses had received training in travel medicine, often through study days run by vaccine manufacturers. The internet was frequently used for information during travel consultations (84.8%) and NaTHNaC's on‐line and telephone advice resources were highly rated. Following YF training, 95.8% of attendees expressed improved confidence regarding YF vaccination issues. There was excellent adherence to vaccination standards: ≥94% correctly stored vaccines, recorded refrigerator temperatures, and maintained YF vaccination records.
Conclusions In the 4 years since institution of the NaTHNaC program for YFVCs, there has been improved adherence to basic standards of immunization practice and increased confidence of health professionals in YF vaccination. The NaTHNaC program could be a model for other national public health bodies, as they establish a program for YF centers.
Yellow fever (YF) is a mosquito‐borne flavivirus infection endemic in parts of Africa and South America. It is a viral hemorrhagic fever with a case‐fatality rate of 20% to 50%.1 The World Health Organization (WHO) reports approximately 1,500 cases each year. It is likely that this is an underestimate, as many YF infections will go undetected or be attributed to other diseases.2
Vaccination of the international traveler against YF involves a complex decision‐making process due to changes in the epidemiology of YF risk and rare, but potentially severe and life‐threatening, adverse events following vaccination.3–7 In addition, an increase in clinical queries about travelers with special health needs going to areas at risk of YF transmission, has been noted.8 Of the 58.6 million trips abroad made by UK residents in 2009 (UK population of 61.8 million), it is estimated that 820,000 travelled to YF‐risk countries.9 Each of these issues necessitates that centers which administer YF vaccine carry out an accurate risk assessment that balances the traveler's itinerary and health status with the safety of the vaccine. Dealing with these complex decisions can be a challenge to YF centers.
In England, the Department of Health designated yellow fever vaccination centers (YFVCs) until July 2003, when they transferred this function to NaTHNaC, a public health body charged with protecting the health of British travelers. In 2005, NaTHNaC established a program of registration, training, clinical standards, and audit for YFVCs following the mandate of International Health Regulations (IHR) (2005): “State parties shall designate specific yellow fever vaccination centers within their territories to assure the quality and safety of the procedures and materials employed.”
10 Part of this program includes a 12‐point Code of Practice with which YFVCs are obliged to comply (Table 1).11 Deviation from these standards could result in the de‐designation of a center. NaTHNaC finalized legislative authority for their program in England in 2005, and extended its responsibility for YFVCs in Wales also in 2005, and in Northern Ireland in 2007.12–14 For YFVCs in Scotland, Health Protection Scotland has a similar program based on the NaTHNaC model.15
1. Only yellow fever (YF) vaccines approved by World Health Organization (WHO) will be administered at the YFVC.
2. Vaccines will be administered only by a qualified medical practitioner (working at the center) or by a nurse or other suitably qualified person (working at the center).
3. Facilities for administering and storing vaccines will conform to acceptable standards.
4. The YFVC will be responsible for developing policies and ensuring staff are appropriately trained to advise travelers in situations in which YF vaccine should be administered.
5. A health professional from each proposed YFVC will attend a NaTHNaC‐sponsored YF training session before designation is granted, and therefore once every 2 years.
6. Appropriate records of vaccination will be maintained for 10 years following each YF vaccination. In the event of a closure of a YFVC, records pertaining to YF vaccination must be archived according to local guidelines.
7. The International Certificate of Vaccination or Prophylaxis (ICVP) will be completed and signed by the vaccinator in accordance with IHR (2005).
8. The administering YFVC is responsible for the reporting and follow‐up of all vaccine‐associated adverse events. Vaccine‐associated adverse events will be reported to the Medicines and Healthcare Regulatory Agency (MHRA).
9. Annual returns of vaccine utilization will be returned to NaTHNaC electronically or by post on the Annual Return form.
10. NaTHNaC will be notified immediately of any changes at the center that might affect its designation, including changes to its address.
11. The YFVC agrees to undertake assessment and audit of their practice as may be required by NaTHNaC. Representatives of NaTHNaC will be given access to the YFVC or may request copies of YFVC records to ensure that a YFVC is complying with the relevant requirements.
12. A YFVC must renew its designation status on an annual or biennial basis. A fee is payable to retain designation status.
The overall goal of NaTHNaC's program for YFVCs is to improve the standard of care for travelers receiving YF vaccination. There are approximately 3,500 YFVCs in England, Wales, and Northern Ireland (EWNI), and more than a third of General Practices in EWNI are yellow fever centers, so any interventions made for YFVCs should positively impact travel medicine (TM) practice as a whole.16
In late 2004 (completed in 2005), prior to rolling out their program, NaTHNaC surveyed existing YFVCs in England. This was to establish the level of practice and determine the training and resources needs of centers.17 The results from this survey highlighted that training should be developed to reinforce best practice in vaccination and improve health professionals' knowledge about YF. The call for heightened training and standards of YFVCs has been made by the WHO in IHR (2005),
10 by the US Centers for Disease Control and Prevention (CDC),
18 and in the literature.16,19–22
The objectives of this study were threefold: to reassess the practice of YFVCs 4 years after institution of the NaTHNaC program, to identify areas for ongoing support, and to assess the impact of the NaTHNaC program.
A questionnaire for YFVCs in EWNI was designed using Survey Monkey® and was piloted by selected travel clinics. The questionnaire included questions on: type of practice, administration of less common travel vaccines (rabies, Japanese encephalitis, tick‐borne encephalitis, and BCG), training of staff, vaccine storage and patient record keeping, access to and use of travel health information, evaluation of the NaTHNaC YF training program, and ongoing resource and training needs. Both closed (dichotomous and multiple‐choice) and free text questions were employed.
In July 2009, all YFVCs (n = 3,465) in EWNI were requested to complete the questionnaire. They were informed via a newsletter sent to YFVCs, on the NaTHNaC website, by email and for centers without known email addresses, by post. Email and postal reminders were sent out over a period of 4 months. Centers could complete the questionnaire electronically or print it and return it by post. YFVCs were informed that their responses would be analyzed in aggregate and not linked to individual centers.
Responses received by post were entered manually into Survey Monkey®. Results were exported into Microsoft Excel® for data cleaning, and data analyzed in STATA 9®. Free text answers were reviewed and grouped into new or existing answer categories. Data were analyzed using chi‐squared tests, tests of proportions, and correlation coefficients.
Where possible, responses reported in this current survey were compared qualitatively to those from the 2005 survey with description of trends.17
Of the 3,465 YFVCs in EWNI in July 2009, a total of 1,454 centers responded to the questionnaire, with 1,438 centers completing the entire survey (41.5%). Response rates to individual questions ranged from 72.6% to 99.9%. The proportion of YFVCs completing questionnaires by geographic area (postcode area) was relatively uniform with 71.6% of areas having a completion proportion between 31 and 50%; 92.9% of responses were from YFVCs in England, comparable to the percent of all YFVCs in England which was 90.0%.
Current Practice of YFVCs
Practice Types and Roles of Healthcare Personnel
Most YFVCs that responded were General Practices (GP) (87.4%), and the person completing the questionnaire was usually the nurse responsible for the YFVC (41.8%) or a practice nurse working in the YFVC (43.0%) (Table 2). Nearly all YFVCs (97.0%) had one or more nurses who administered YF vaccine; only 24.2% of centers had one or more physician administering YF vaccine (p < 0.0005). In addition, 97.0% of centers had nurses who advised travelers, whereas only 36.5% of centers had physicians advising travelers (p < 0.0005). A reduction was observed in the proportion of physicians administering YF vaccine (24.2% vs 48.7%) and advising travelers (35.5% vs 52.6%) compared to the baseline study. In the UK, nurses usually work under the specific direction of the lead physician.
Practice type and roles of those completing the questionnaire for yellow fever vaccination centers (YFVCs) in England, Wales, and Northern Ireland
Number (%) current study
Number (%) 2005 study*
Occupational Health Center
Private Travel Clinic
Private Health Facility
Role of responder
Nurse responsible for YFVC
↵* The 2005 study surveyed YFVCs prior to initiation of NaTHNaC's program.17
↵† There were a total of 3,465 YFVCs; the response rate for completion of the entire questionnaire was 41.5% (1,438/3,465) for practice type and 41.3% (1,432/3,465) for role of responder.
Vaccine Administration and Travel Medicine Services
There was a wide range in the number of doses of YF vaccine given by YFVCs (Figure 1). The median number of doses was 50 per year [inter‐quartile range (IQR) 30–75 doses], more than the baseline survey (median of 35 doses per year). The number of doses of YF vaccine given differed significantly by clinic type (p < 0.0005) with private travel clinics administering proportionally more than all other clinic types.
Frequency of yellow fever vaccination centers (YFVCs) by the annual number of yellow fever doses given at each YFVC. The median number of doses given was 50 (IQR 30–75). The response rate for this question was 92.4% (1,344/1,454).
The number of TM patients seen at each practice or clinic varied considerably; the median number was 267 per year (IQR 150–500 patients per year). Specialty vaccines used for travel were offered at a similar frequency compared with the 2005 survey (Table 3). TM consultations were most often between 11 and 20 min in length (67.3% of YFVCs). In addition to pre‐travel health consultations, 72.6% of centers gave telephone advice.
Travel medicine services offered in yellow fever vaccination centers (YFVCs)
Number (%) current study
Number (%) 2005 study*
Vaccines offered other than yellow fever vaccine
Number of travel medicine sessions per week
Time allocated per consultation
Travel medicine services
Travel health supplies for purchase
Association with a clinical laboratory
Research in travel medicine
↵* The 2005 study surveyed YFVCs prior to initiation of NaTHNaC's program.17
Training of Personnel
YFVCs were asked about TM training. Nurses had received some training in 96.7% of YFVCs compared with physicians in 32.2% of centers (p < 0.0005). The number of physicians with TM training was less than in the baseline survey, where 56.6% of physicians had such training. The most common type of training for nurses were study days run by vaccine manufacturers (87.0% of nurses had attended one), compared to 40.0% in the baseline survey. Self‐study was reported by 60.8% of nurses (Figure 2), and was the most common form of training for physicians (51.7%), followed by vaccine manufacturer training days (44.6%). Forty percent of physicians attended vaccine manufacturer training days in 2005.
Types of travel medicine training attended by physicians and nurses who worked in yellow fever vaccination centers (YFVCs). Abbreviations and explanations: MSc, Master of Science (a postgraduate degree); Diploma level course [a 1‐year course awarded by the Royal College of Physicians and Surgeons (Glasgow)]; Foundation level course [a 6‐month course awared by Royal College of Physicians and Surgeons (Glasgow)]; Short course (courses of a few days' duration).
Few nurses or physicians had membership of the Faculty of Travel Medicine (Royal College of Physicians and Surgeons, Glasgow)
23 (3.6 and 3.3%, respectively), or had passed the International Society of Travel Medicine Certificate of Knowledge examination in TM (1.5 and 1.9%, respectively)
; 7 to 13% had completed a diploma level course (a year of distance learning in TM).
Access and Use of Sources of Travel Medicine Information
All but one YFVC reported having internet access at their center, and nearly all of these centers had it available during a TM consultation (98.7%). Of those who did have internet access during the consultation, 84.8% used it for each patient, compared to the 44.0% who reported using it for each patient in the baseline survey. The internet was used during a consultation for country recommendations (95.9% of YFVCs), general TM information (83.1%), information sheets on travel diseases (80.5%), and information on global disease outbreaks (65.1%). The most frequently accessed websites were the NaTHNaC website (87.8% of respondents) and Health Protection Scotland's TRAVAX website (73.5%). In contrast, the NaTHNaC website was used by only 18% of YFVCs in 2005.
Regarding printed resources, the Department of Health book, Immunisation against Infectious Disease, which covers immunization guidelines for the UK (92.9%), and the British National Formulary, an information source about the use of medicines (71.9%), were the most widely used resources. Vaccine charts in health professional periodicals were used by only 29.5% compared with 73.7% in the baseline survey. The NaTHNaC telephone advice line was the most commonly used telephone line (77.1%), a marked increase from the 14.4% of centers previously using it.
Future Resource and Training Needs
Respondents reported that training courses on travel health topics (69.9%), clinical updates on important travel health issues posted on the NaTHNaC website (68.5%), and access to a website containing travel health information (61.3%) were important training and resource needs (Table 4).
YFVCs were asked about their adherence to some key points of the Code of Practice (Table 1), and to evaluate aspects of the NaTHNaC program to assess the impact of the program on their practice.
Vaccine Storage, Record Keeping, and Anaphylaxis
Nearly all YFVCs used a dedicated vaccine refrigerator (either with or without an internal thermometer) (96.6%). Only 3.4% of YFVCs stored vaccines in a domestic refrigerator. This was an improvement from 2005 where 10.7% of centers used a domestic refrigerator.
Nearly all YFVCs recorded the temperature of their fridges at least every working day (98.7%), a required standard. In the 2005 survey 94.6% recorded the temperature at least daily. YFVCs also kept temperature records (99.4%), with 48.3% of them keeping them for at least 10 years (Table 5).
Number of centers that conformed to the Code of Practice standards
Conformed to standards, current study (%)
Conformed to standards, 2005 study* (%)
Response rate, current study (n)
Response rate, 2005 study* (n)
Type of refrigerator
Frequency of recording fridge temperature
Length of time for keeping yellow fever vaccination records
↵* The 2005 study surveyed yellow fever vaccination centers prior to initiation of NaTHNaC's program.17
Patient records on general vaccinations were usually recorded in an electronic patient database (64.4 %), and most YFVCs kept the records permanently (75.6%). In contrast, YF vaccination records were usually recorded in patient notes with separate YF records also being kept (75.3%). YF vaccine records were kept by 94.2% of centers for at least 10 years, the required standard (Table 5). In 2005, 82.2% of centers kept records for at least 10 years.
Evaluation of NaTHNaC Resources and Training Program
Respondents were asked to evaluate a selection of NaTHNaC resources: the national telephone advice line, and website items including country information pages, TM and disease information sheets, information on travel health developments (Clinical Updates), and global disease outbreaks (Outbreak Surveillance Database). Between 77.0 and 86.6% of respondents rated each resource as either “useful” or “very useful,” the two highest ratings on a 5‐point scale.
When asked to evaluate the NaTHNaC training program, 95.8% of those who attended either a full or half day YF training session (n = 1,326), stated that the training improved their confidence regarding issues surrounding YF vaccine. In addition, 68.5% (CI 65.9%–71.0%) of YFVCs reported making changes to their practice following training.
This survey of YFVCs in EWNI was performed 4 years after the initiation of the NaTHNaC program of registration, training, clinical standards, and audit for YFVCs. It provides an update on the clinical practice of YFVCs, identifies ongoing needs of YFVCs, and assesses the impact of NaTHNaC's program on centers.
The number of YFVCs in EWNI has remained steady at 3,400 to 3,500 since implementation of the program (data not shown). With the institution of registration and training requirements and their associated fees, plus the requirement to adhere to the 12‐point Code of Practice (Table 1),
11 there has been no decline in the number of practices. This suggests that NaTHNaC's introduction of standards has not been perceived as a burden for practices, but possibly as a way to demonstrate compliance with a national standard and to improve the governance of a YFVC. The importance of standards in the practice of TM has been emphasized by international health bodies.10,18
This survey has determined that in EWNI, YF vaccination is given predominantly in the General Practice setting, and practice nurses continue to be the main providers of YF‐risk assessment, advice, and vaccination, reflecting the overall practice of TM in the UK.25,26 This study also suggests a decline in the involvement of physicians in TM between 2005 and 2009, with fewer physicians administering YF vaccine and fewer advising travelers. It could be that physicians are concentrating on other clinical responsibilities within their practice and leaving TM to the nursing staff. However, this could be a reflection of those centers that completed the survey.
The median number of YF vaccine doses administered each year was 50 in this survey. This is an increase from 2005, when the median number was 35 doses. Without knowing the total number of doses of YF vaccine sold in the EWNI, it is difficult to determine if this is a true increase over 2005. YFVCs also estimated that they saw a median of 267 TM patients per year, with TM consultations performed in 20 min or less at 73.9% of centers.
The information from this survey gives a picture of TM practice in YFVCs in EWNI: the majority of YFVCs are in the setting of General Practice, the service is nurse‐led, consultations are delivered in 20 min or less, and relatively few travelers are seen—approximately 5 per week, with one of those receiving YF vaccination. Having TM within General Practice is an advantage for travelers as they have ready access to the service. However, other demands could mean that there is not enough time during the TM consultation to undertake a complete risk assessment of the journey and convey and administer risk management interventions. In addition, depending upon practice location and population served, relatively few travelers may be seen. This raises questions about maintaining expertise and competency. Having a national center that defines standards of practice and provides real‐time advice and resources could help YFVCs give competent care for their patients.
There remain ongoing needs for YFVCs in the areas of training and resources. Respondents considered that courses on travel health topics were the most important training and resource need. Much of the current training received by physicians and nurses is delivered on study days sponsored by vaccine manufacturers; 87% of nurses and 45% of physicians had attended this type of training. These percentages are higher than in the 2005 survey. It is important that training in TM is separated from any potential bias; however, this can be difficult when nonsponsored training presents a cost to the attendee. Having other incentives such as continuing education credits from UK Royal Colleges that contribute to maintenance of professional competence and development of expertise in TM, may help balance this. It is also important that training can be obtained with the least disruption to practice. Providing the option for on‐line training would allow nurses and physicians to complete this on their own time, avoiding travel costs and the need for time off from work. NaTHNaC, while currently offering only training in YF, has added continuing education credits to its course from the Royal College of Nursing, and is developing on‐line training capability as well as additional modules in TM.
Higher qualifications such as postgraduate degrees or higher education diplomas and certificates in TM were not obtained by many health professionals working in YFVCs. Whether higher levels of training and recognition of knowledge in TM translate to improved practice in the clinical setting remains to be determined.
Practitioners are also looking for reliable, up‐to‐date information for country recommendations and for outbreaks of disease occurring at their travelers' destinations. Several commercial and authoritative national, international, and independent sources provide this. Examples of independent, open access disease outbreak information sources are the CDC Travel Notices,
27 the WHO Disease Outbreak News,
28 HealthMap's global health information website,
29 the Program for Monitoring Emerging Diseases (ProMED),
30 and the NaTHNaC Outbreak Surveillance Database.31 These are all web‐based resources, emphasizing the need for those practicing TM to have access to the internet for each consultation, something that most (85%) of the YFVCs in EWNI did. This is nearly double the number that reported using the internet for each consultation in the 2005 survey (44%) indicating the growth of point of care information technology.
NaTHNaC has developed a combination of resources for TM practitioners that include a website with country‐specific and outbreak information (rolled out in 2007), a national telephone advice line (since 2003) dedicated to health professionals, and a definitive TM text: the 2010 edition of Health Information for Overseas Travel. This book complements NaTHNaC's website information and provides support for the TM consultation. Compared with 2005, in 2009 YFVCs most frequently accessed the NaTHNaC website and called its national advice line compared with other resources. In addition, more authoritative print resources were used, eg, the Department of Health immunization book and the British National Formulary, compared with the use of the less comprehensive vaccine charts.
As a measure of practice improvement, YFVCs were asked about adherence to standards. Since initiation of the NaTHNaC program, adherence to standards of immunization practice has improved and confidence levels of health professionals in YF vaccination have increased.32 There was improvement in proper vaccine storage, recording of fridge temperature records, and maintenance of patient vaccination records. Individuals who had undergone training also expressed improved confidence in YF vaccination issues and had made changes within their YFVC.
Increased access to up‐to‐date resources, both on‐line and text, improved adherence to core standards of practice, and improved confidence of providers is expected to translate to more consistent and better care for the international traveler who visits their GP surgery or private TM clinic, an important goal for the practice of TM.10,18,21,23,33
The major limitation of this study is that the response rate was lower than in the baseline study. It is not possible to quantify the selection biases present in this study, however, the distribution of YFVCs completing the questionnaire was representative of the complete database in terms of location, size, and type. As potential explanations for the lower response rate, the questionnaire was administered when there were extensive demands upon health professionals caused by pandemic influenza, and response to the 2005 survey was obligatory if the center wished to continue practising as a YFVC. Questionnaires were completed anonymously and were not matched in the 2005 and 2009 surveys, meaning that results from this survey could not be directly compared with the 2005 survey. While this limits the ability to measure improvements, anonymity was chosen to encourage YFVCs to respond and to complete the survey honestly. Despite this limitation, trends have been identified and discussed.
There is also the question whether self‐reporting is a valid tool for unbiased data capture. Improvements to clinical practice often begin with a standard being implemented. Self‐reporting is then used to assess compliance, with a more formal audit of practice based on these results. In person audits of YFVCs were not possible for this study given the resources available. However, on‐line surveys can deliver comparable results to more traditional methods.34 A more detailed audit of clinical decision making is planned for all YFVCs in 2012.
It is possible that other influences within the field of TM, such as availability of new resources, could have contributed to the observed improvements in practice. However, the introduction of core standards by NaTHNaC, and the training and ongoing sources of support that NaTHNaC provide are likely to have improved YF practice in EWNI. Determining if adherence to standards translates to improved care in TM is an important research question.
Only a few countries have established national programs for YF vaccination and, unlike the NaTHNaC program, most have not tied designation status to standards, education, and audit.20–22 With international efforts to improve the quality of care received in TM practice, a model such as that developed by NaTHNaC could be considered by other countries, as they aim to comply with the IHR (2005) request to designate specific YFVCs.
Declaration of Interests
The authors state that they have no conflicts of interest.
NaTHNaC thanks the dedicated travel medicine professionals who deliver NaTHNaC's training to YFVCs (Shirley Bannatyne, Lynda Bramham, Carolyn Driver, Norma Evans, Sandra Grieve, Joanna Lowry, Kath Lynch, Alison Jenkins, Sarah Lang, Cate Riley, and Dr Steve Riley). We also thank the administration staff who provide the logistical support for the YFVC program (Geraldine Oliver and Yetunde Ibitoye), and former staff who helped to develop the program for YFVCs (Dr Gil Lea, Rose Tucker, and Stella Bailey).
The National Travel Health Network and Centre charges a registration fee for yellow fever vaccination centers (YFVCs). This fee contributes to running the NaTHNaC program for YFVCs and to the general operating budget of this not‐for profit organization.
, et al.Calls to a national travel health advice line—information from the National Travel Health Network and Centre (NaTHNaC).Presented at 12th Conference of the International Society of Travel Medicine, Boston, 2011.
National Travel Health Network and Centre. Designation of yellow fever vaccination centres, England, Wales and Northern Ireland. Information Pack. London: National Travel Health Network and Centre, 2009:1–35.Available at: http://www.nathnac.org/pro/documents/YFInfoPack.pdf(Accessed 2011 Oct 27).
Chief Medical Officer. Designation and administration of yellow fever vaccination centres, HSS (MD) 21/2007. 2007. Belfast: Department of Health, Social Services and Public Safety.Available at: http://www.dhsspsni.gov.uk/hss_md_21-2007.pdf(Accessed 2011 Oct 27).
Centers for Disease Control and Prevention. Centers for Disease Control and Prevention travel notices. Atlanta, GA: Centers for Disease Control and Prevention, 2011. Available at: http://wwwnc.cdc.gov/travel/default.aspx(Accessed 2011 Oct 27).
International Society for Infectious Diseases. The Program for Monitoring Emerging Diseases (ProMED). International Society for Infectious Diseases, 2011. Available at: http://www.promedmail.org/(Accessed 2011 Oct 27).
International Society of Travel Medicine. About ISTM. Mission statement. Atlanta, GA: International Society of Travel Medicine, 2011. Available at: http://www.istm.org/WebForms/About/(Accessed 2011 Oct 27).