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Vaccine 32 (2014) 4993–4999

Contents lists available at ScienceDirect

Vaccine

j our na l ho me page: www.elsev ier .com/ locate /vacc ine

accination status, knowledge and awareness towards hepatitis Bmong students of health professions in Vientiane, Lao PDR

olakoth Pathoumthonga,1, Phonepaseuth Khampanisonga,1, Fabrice Quetb,c,atthanaphone Latthaphasavangb,d, Vimalay Souvongb, Yves Buissonb,∗

University of Health Sciences, Vientiane, Lao Democratic People’s RepublicInstitut de la Francophonie pour la Médecine Tropicale (IFMT), Vientiane, Lao Democratic People’s RepublicUMR 1094 (Université de Limoges/Inserm/CHU de Limoges) Neuroépidémiologie Tropicale (NET), Limoges, FranceDepartment of Infectious Diseases, Mahosot Hospital, Vientiane, Lao Democratic People’s Republic

r t i c l e i n f o

rticle history:eceived 18 March 2014eceived in revised form 5 June 2014ccepted 8 July 2014vailable online 24 July 2014

eywords:ealth-care workersepatitis Bepatitis B vaccineaccine coveragetudentsao PDR

a b s t r a c t

Health care workers (HCW) are a population at high risk of hepatitis B virus (HBV) infection, especially inendemic countries such as Lao PDR. Effective vaccines are available since over 10 years, but many HCWsare not aware of the risk of infection and are still not immunized against hepatitis B. This study aimed toassess immunization coverage against hepatitis B among the students of the University of Health Sciences(UHS) of Lao PDR in 2013 and to look for the causes of non-vaccination. A cross-sectional survey wasconducted by self-administered questionnaire on a representative stratified sample of each academicyear in each faculty. In total, 961 questionnaires were collected, Basic Sciences: 143, Medicine: 167,Pharmacy: 148, Dentistry: 139, Nursing Sciences: 159, Medical Technology: 99, and Postgraduate Studies:106. Respondents were predominantly female (59.1%), mean age 25.1 ± 7.0 years, single (76.3%), from theprovinces (68.0%), of the Lao Loum ethnic group (84.4%). Among them, 21% were fully vaccinated againsthepatitis B and 9.5% partially. Immunization coverage rates were significantly higher among women(p = 0.01), students aged over 25 years, married or belonging to the post-graduate faculty (p < 0.001).The most common reason (38.6%) given for non-vaccination was not knowing where to get vaccinated.Knowledge about hepatitis B, scored from 0 to 5, was poor (0–1) for 86.5% of the students, but 77.5% were

aware of the hepatitis B vaccine. The knowledge scores were significantly higher for students aged over 25years, married or post-graduated (p < 0.001). Vaccination coverage against hepatitis B is dramatically lowamong students of health professions in Laos, largely because of their lack of knowledge and awareness.Upon admission to the University, all future HCWs should receive information about the occupationalrisks of blood-borne viruses transmission and be encouraged to get vaccinated against hepatitis B.

. Introduction

Hepatitis B virus (HBV) infection is a major occupational hazardor health care professionals in that it is considered to be 2–10 timesigher than in the general population [1]. In most cases, exposure

s due to accidental contact with human blood or body fluids fromsymptomatic carriers of HBV. From prospective studies amongealth care workers (HCWs), the average risk of transmission after

∗ Corresponding author. Tel.: +33 6 47 03 45 87.E-mail addresses: pkolakoth@gmail.com (K. Pathoumthong),

pnzpaul@gmail.com (P. Khampanisong), fabrice.quet@unilim.fr (F. Quet),yllaos@gmail.com (V. Latthaphasavang), vimalay.souvong@yahoo.comV. Souvong), yvesbuisson@hotmail.com (Y. Buisson).

1 These authors contributed equally to this work.

ttp://dx.doi.org/10.1016/j.vaccine.2014.07.022264-410X/© 2014 Elsevier Ltd. All rights reserved.

© 2014 Elsevier Ltd. All rights reserved.

a percutaneous exposure to infected blood has been estimatedapproximately 0.3% for HIV, 1.8% for HCV and 6–30% for HBV[2]. Injuries with contaminated injection devices are common indeveloping countries due to the lack of knowledge about controlpractices, the lack of resources for sterilization and buying dispos-ables and the cultural preferences for injectable treatments [3].

With nearly 130 million chronic HBV carriers, the SoutheastAsian region has one of the highest endemic levels in the world,perinatal route being the main mode of transmission. The rateof seroprevalence of HBV surface antigen (HBsAg) ranges from 1to 10% depending on the countries and the control programmesimplemented [4]. However, despite the childhood immunization

programmes initiated in the last two decades, HBV continues to cir-culate in the populations, the disease being more observed in adultsand adolescents born before the introduction of vaccination pro-grammes [5]. Therefore, the risk of transmission is high for health

4994 K. Pathoumthong et al. / Vaccine 32 (2014) 4993–4999

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ig. 1. Caption sampling design in the seven faculties of the University of Health Scach year of study in each faculty (study years yellow coloured include hospital int

orkers in countries where the HBV carrier rate exceeds 8% of theeneral population.

Lao PDR is one of the least developed countries of ASEAN withn estimated population of 6.4 million, of which 66.8% is dispersedn rural areas and 27.6% live below the poverty line [6]. There is

large ethnic diversity, commonly simplified into three groups:ao Loum or lowland Lao (66%), Lao Theung or midland Lao (24%)nd Lao Soung or hill tribes (10%). The HBsAg seroprevalence inao PDR is estimated by reference to the rate of 8.7% determined inne study from 13,897 blood donors between 2003 and 2005 [7].erinatal mother-to-child transmission being the most commonoute of infection, the Lao government decided to implement the

HO recommendations and improved the extended programme ofmmunization by introducing the birth dose of hepatitis B vaccineince 2004 [8]. In addition, hepatitis B vaccination is recommendedor all people at risk, especially for the occupationally exposed sub-ects such as HCWs, but it then must be paid by the applicant.owever, it should be considered as a prerequisite for all studentsho intend to pursue a profession in health care. But there is no sys-

ematic vaccination of HCWs planned, neither during their trainingor at the end of their studies. A preliminary survey conducted in009 among 1054 students from the University of Health SciencesUHS) in Lao PDR revealed that only 18% of them were vaccinatedgainst hepatitis B [unpublished data].

The present study aimed to determine the hepatitis B vaccineoverage among students from different faculties of the USS in013 and to identify factors for non-vaccination by assessing theirnowledge about hepatitis B and awareness of risks which they arexposed.

. Methods

.1. Study type and population

The UHS is composed by seven faculties, namely Faculty ofasic Sciences, Faculty of Medicine, Faculty of Pharmacy, Faculty of

s: number of students randomly selected based on the total number of students inps).

Dentistry, Faculty of Nursing Sciences, Faculty of Medical Technol-ogy and Faculty of Postgraduate Studies. The hospital internshipsare programed from the second year for Nursing sciences and Med-ical technology students, from the third year for dentistry students,from the fourth year for medical students, from the fifth year forpharmacy students and are part of the two years of postgraduatestudies (Fig. 1).

A cross-sectional survey was conducted in each academic yearof the seven faculties. A preliminary study conducted in 2009had assessed the vaccine coverage of UHS students around 15%.According to the total number of students, theoretical samplesrepresentative of each faculty were calculated using OpenEpi Cal-culators (http://www.openepi.com/) with an accuracy of 5%. A totalof 961 students were needed, i.e. 143 in basic sciences, 167 inmedicine, 148 in pharmacy, 139 in dentistry, 159 in nursery, 99in medical technology and 106 in postgraduate studies (Fig. 1). Thenumber of students to be included from each year of study was thenproportionally calculated for each faculty. Starting with a name ran-domly selected, a student every five names was extracted from thealphabetical list until the required number of subjects was reached.In case of refusal, the immediate following student on the list wassolicited.

2.2. Data collection

A standardized questionnaire, written in Lao language, wasself-administered by the selected students. Divided in four parts(sociodemographic data, knowledge, awareness and vaccinationstatus against hepatitis B), it was presented as multiple choicequestions, except for the knowledge test consisting of five openquestions on (1) the agent of hepatitis B, (2) the mode of transmis-sion, (3) the risk factors, (4) the symptoms of acute hepatitis and

(5) the complications of hepatitis B. Knowledge was scored from 0to 5, with one point awarded for each correctly answered question.The survey data sheets were entered through a Microsoft Accessdedicated application

K. Pathoumthong et al. / Vaccine 32 (2014) 4993–4999 4995

Table 1Socio-demographic characteristics and vaccination status against hepatitis B of the students from the University of Health Sciences of Laos according to their faculty.

Totaln = 961 (%)

Faculties

Basic Sciencesn = 143 (%)

Medicinen = 167 (%)

Pharmacyn = 148 (%)

Dentistryn = 139 (%)

NursingSciencesn = 159 (%)

Medicaltechnologyn = 99 (%)

PostgraduateStudiesn = 106 (%)

GenderMale 393 (40.9) 62 (43.4) 84 (50.3) 44 (29.7) 56 (40.3) 40 (25.2) 60 (60.6) 47 (44.3)Female 568 (59.1) 81 (56.6) 83 (49.7) 104 (70.3) 83 (59.7) 119 (74.8) 39 (39.4) 59 (55.7)

Age (years)< 20 106 (11.0) 54 (37.7) 2 (1.2) 22 (14.9) 10 (7.2) 8 (5.0) 10 (10.1) 0 (0.0)20–25 587 (61.1) 57 (39.9) 144 (86.2) 116 (78.4) 119 (85.6) 76 (47.8) 68 (68.7) 7 (6.6)>25 268 (27.9) 32 (22.4) 21 (12.6) 10 (6.7) 10 (7.2) 75 (47.2) 21 (21.2) 99 (93.4)

Marital statusSingle 733 (76.3) 115 (80.4) 150 (89.8) 137 (92.6) 125 (90.0) 87 (54.7) 80 (80.8) 39 (36.8)Married 221 (23.0) 28 (19.6) 17 (10.2) 11 (7.4) 13 (9.3) 66 (41.5) 19 (19.2) 67 (63.2)Divorced 7 (0.7) 0 (0.0) 0 (0.0) 0 (0.0) 1 (0.7) 6 (3.8) 0 (0.0) 0 (0.0)

OriginCapital 307 (32.0) 40 (28.0) 45 (26.9) 34 (23.0) 55 (39.6) 64 (40.3) 22 (22.2) 47 (44.3)Province 654 (68.0) 103 (72.0) 122 (73.1) 114 (77.0) 84 (60.4) 95 (59.7) 77 (77.8) 59 (55.7)

Ethnic groupLao Loum 811 (84.4) 123 (86.0) 136 (81.4) 129 (87.2) 119 (85.6) 130 (81.8) 78 (78.8) 96 (90.6)Lao Soung 56 (5.8) 6 (4.2) 10 (6.0) 10 (6.7) 5 (3.6) 13 (8.2) 11 (11.1) 1 (0.9)Lao Theung 94 (9.8) 14 (9.8) 21 (12.6) 9 (6.1) 15 (10.8) 16 (10.0) 10 (10.1) 9 (8.5)

Hepatitis B vaccinationFull 202 (21.0) 18 (12.6) 37 (22.1) 14 (9.5) 13 (9.4) 41 (25.8) 11 (11.1) 68 (64.1)

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Partial 91 (9.5) 17 (11.9) 18 (10.8) 13

No 509 (53.0) 68 (47.5) 89 (53.3) 85

Unknown 159 (16.5) 40 (28.0) 23 (13.8) 36

.3. Statistical analyses

Statistical analyses were done using Microsoft Excel andTATA softwares. Comparisons of percentages were performed byhi-square test or Fisher’s exact test when appropriate. Meansomparisons were made by Student’s t-tests or Mann & Whit-ey tests, as well as ANOVA when more than two means whereompared. Factors statistically associated with the vaccination oftudents against hepatitis B and factors statistically associated withhe awareness of being at risk for hepatitis B were determined byogistical regression. For both regressions, every variable with aevel of significance equal or below 25% in bivariate analyses wasncluded in the initial models. Final models were obtained usingtep-by-step backward elimination method. For all statistical anal-ses a level of significance equal or below 5% was considered asignificant.

.4. Ethics

The study has been approved by the Research Ethics Committeef the UHS. Selected students answered anonymously to the self-uestionnaire. They were free to participate or not in the survey.

. Results

The theoretical sample size was achieved and 961 question-aires were collected. Only 23 students (2.4%) refused to participate

n the survey, 14 of nursing sciences, 5 of pharmacy and 4 ofedical technology, claiming lack of time. The respondents were

redominantly female (59.1%), with a mean age of 25.1 ± 7.0 yearsrange: 17–50 years), most singles (76.3%), originating from therovinces (68.0%) and belonging to the Lao Loum ethnic group84.4%) (Table 1).

.1. Immunization against hepatitis B

Of the 961 students surveyed, 202 had received full immu-ization against hepatitis B (21.0% [CI95: 18.4–23.6]), i.e. at least

15 (10.8) 20 (12.6) 4 (4.0) 4 (3.8) 99 (71.2) 68 (42.7) 66 (66.7) 34 (32.1) 12 (8.6) 30 18.9) 18 (18.2) 0 (0.0)

three doses of vaccine, 91 were partially immunized (9.5% [CI95:7.6–11.4]) with only one or two doses of vaccine, and 159 students(16.5% [CI95: 14.2–18.8]) were unable to say whether they were vac-cinated or not (Table 1). Women were more vaccinated than men(p = 0.01), as well as students aged over 25 years (p < 0.001) andthose who were married (p < 0.001). Significant differences werenoted between the seven faculties of the UHS (p < 0.001): the high-est rate of full hepatitis B vaccine coverage was observed amongpostgraduate students (64.2% [CI95: 54.3–73.2]), followed by nurs-ing students (25.8% [CI95: 19.2–33.3]), medical students (22.2%[CI95: 16.1–29.2]), basic sciences students (12.6% [CI95: 7.6–19.2]),medical technology students (11.1% [CI95: 5.7–19.0]), pharmacystudents (9.5% [CI95: 5.3–15.4]), and dental students (9.4% [CI95:5.1–15.5]). In multivariate analysis, being married compared to sin-gle or being enrolled in the postgraduate studies compared withfaculty of medicine were two factors independently associatedwith a full immunization (Table 2). Conversely, students from theremaining faculties and Lao Soung students were respectively lessvaccinated against hepatitis B than medical and Lao Loum students.

Among students fully (n = 202) or partially (n = 91) vaccinatedagainst hepatitis B, the main motivations were to protect one-self against a serious and potentially fatal disease (23.4%) and thefear of occupational exposure to hepatitis B (22.6%). In contrast,among the unvaccinated students, the main reason alleged fornon-vaccination was that they did not know where to get vacci-nated (Table 3). Among the 668 students not vaccinated (n = 509) orunaware (n = 159) of their vaccination status, 525 (78.6%) intendedto be immunized against hepatitis B. This intention was expressedmainly by students of Postgraduate Studies and Nursing Sciencesfaculties (84.9% each).

3.2. Knowledge about hepatitis B

More than 72% of students surveyed were unable to correctly

answer any of the five questions about hepatitis B and 245 (25.5%)had never heard of it. Of the remaining 716 students, 195 (27.1%)knew the agent of hepatitis B, 66 (9.2%) knew the mode of transmis-sion of HBV, 14 (2.0%) were aware of the risk factors for hepatitis

4996 K. Pathoumthong et al. / Vaccine 32 (2014) 4993–4999

Table 2Factors associated with vaccination of students against hepatitis B: results of a logistical regression.

Variables Univariate analysis Multivariate analysis

cOR CI95% p aOR CI95% p

Faculty (ref: Medicine)Post-graduate studies 4.31 [2.56–7.25] <0.001 2.71 [1.56–4.73] <0.001Basic sciences 0.66 [0.40–1.09] 0.103 0.58 [0.35–0.97] 0.036Dentistry 0.51 [0.30–0.87] 0.013 0.50 [0.30–0.86] 0.012Pharmacy 0.45 [0.27–0.77] 0.003 0.45 [0.26–0.76] 0.003Medical technology 0.36 [0.19–0.69] 0.002 0.33 [0.17–0.62] 0.001Nursing sciences 1.27 [0.80–2.00] 0.306 0.96 [0.59–1.56] 0.878

Marital status (ref: single)Married 3.50 [2.55–4.78] <0.001 2.39 [1.67–3.43] <0.001Divorced 0.53 [0.06–4.41] 0.555 0.59 [0.06–5.35] 0.638

Ethnic group (ref: Lao Loum)Lao Soung 0.60 [0.37–1.01] 0.053 0.57 [0.33–0.98] 0.041Lao Theung 0.52 [0.26–1.21] 0.054 0.59 [0.29–1.23] 0.159

Age (ref: <20 years)>25 years 3.74 [2.23–6.25] <0.00120–25 years 0.96 [0.59–1.58] 0.879

Study year (ref: first year)Second year 1.54 [1.05–2.26] 0.026Third year 0.83 [0.54–1.29] 0.415Fourth year 0.90 [0.57–1.44] 0.670Fifth year 0.77 [0.46–1.28] 0.308Sixth year 1.02 [0.59–1.74] 0.952

Gender (ref: male)

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OR: crude odd ratio; CI95%: confidence interval 95%; p: p-value; aOR: adjusted odd

, 50 (7.0%) of the main symptoms and 129 (18.0%) of the com-lications. The level of knowledge was independent of gender andthnic group, but was significantly higher among students agedver 25 years, married, or pursuing Postgraduate studies. Medicaltudents ranked second but nearly half of them had a total score ofero. Nevertheless, knowledge scores increased significantly withhe number of years of study at the UHS (Table 4).

About the knowledge upon vaccination, 77.5% of students sur-eyed were aware of the vaccine against hepatitis B, the highestates being recorded in students over the age of 25 years (p < 0.001),he married subjects (p < 0.001), and the postgraduate studentsp < 0.001). Their main sources of information were the university64.4%), the media (46.7%), the friends (20.0%), the relatives (11.8%)nd the hospitals (4.3%).

.3. Awareness of being at risk for hepatitis B

Only a minority of students (37.0% [CI95: 34.0–40.2]) consideredeing at risk for HBV infection.

able 3easons mentioned for vaccination and non-vaccination against hepatitis B (severalossible answers).

Vaccination (293 vaccinated students) No (%)Hepatitis B is a serious disease that can be fatal 151 (23.4)Fear of occupational exposure to hepatitis B 146 (22.6)Prevention of liver cancer 123 (19.0)Vaccination against hepatitis B is recommended by WHO 101 (15.7)To follow the advice given by parents 71 (11.0)To set a good example in the family 43 (6.7)Other 10 (1.6)

Non-vaccination (509 unvaccinated students) No (%)Do not know where to get vaccinated 236 (38.6)The vaccine is too expensive 96 (15.7)Fear of side effects of the vaccine 84 (13.7)Fear of needles 51 (8.3)No fear of catching hepatitis B 34 (5.6)The vaccination is not very effective 20 (3.3)Other 91 (14.9)

0.209

This feeling was more developed in subjects aged over 25years (p < 0.001), married (p < 0.001), Lao Loum (p = 0.02). Higherpercentages of students belonging to the faculties of medicineand postgraduate studies were aware of the risk of hepatitisB, respectively 58.7% and 58.5% of students; in contrast, only13.1% of students from the faculty of medical technology wereaware (p < 0.001). For all students, this perception was significantlystrengthened with the number of years at UHS (Table 5). In mul-tivariate analysis, factors independently associated with a greaterawareness of being at risk were the number of study years (abovethe third year compared to the first year) and the age (being olderthan 25 years compared to students less than 20 years). Converselysome factors were independently associated with a lower aware-ness of the risk to be infected, as the ethnic group (Lao Soung lessaware compared to Lao Loum), and the faculty (pharmacy, den-tistry and medical technology students less aware than medicinestudents) (Table 5).

4. Discussion

The main objective of this survey was to evaluate the primaryprevention of hepatitis B in the high-risk population that are stu-dents of the UHS in Laos. Several studies have focused on theimmune status of HCWs against hepatitis B, but relatively few arededicated to students in training for the health professions, whilevaccination should precede exposure to occupational risks of HBVinfection. This study, conducted in a country of high prevalence ofhepatitis B, allowed to interview a total sample of 961 students, rep-resentative for each of the seven faculties of the UHS. It highlightsan overall rate of 21% vaccination coverage, considering that onlysubjects who received a standard immunization schedule with atleast three doses of recombinant vaccine against hepatitis B werefully vaccinated [9].

Significant variations are observed between faculties. The high-

est rate of vaccination coverage (64.2%) is recorded in the Faculty ofPost-graduate Studies which welcomes students who have alreadycompleted five to six years of university studies. Students areenrolled for residency training programme in medical specialties,

K. Pathoumthong et al. / Vaccine 32 (2014) 4993–4999 4997

Table 4Knowledge scores (rated from 0 to 5) about hepatitis B of the students from the University of Health Sciences.

Variable N (%) Knowledge scores pa

0 1 2 3 4 5 Mean ± SD699 (72.7) 132 (13.7) 79 (8.2) 42 (4.4) 8 (0.8) 1 (0.1)

GenderMale 393 (%) 282 (71.8) 58 (14.8) 29 (7.4) 19 (4.8) 4 (1.0) 1 (0.2) 0.49 ± 0.93 0.521Female 568 (%) 417 (73.4) 74 (13.0) 50 (8.8) 23 (4.1) 4 (0.7) 0 (0.0) 0.46 ± 0.87

Age<20 years 106 (%) 100 (94.3) 3 (2.8) 2 (1.9) 1 (1.0) 0 (0.0) 0 (0.0) 0.09 ± 0.43 <0.00120–25 years 587 (%) 476 (81.1) 67 (11.4) 30 (5.1) 11 (1.9) 3 (0.5) 0 (0.0) 0.29 ± 0.70>25 years 268(%) 123 (45.9) 62 (23.1) 47 (17.5) 30 (11.2) 5 (1.9) 1 (0.4) 1.01 ± 1.15

Marital statusSingle 733 (%) 577 (78.7) 86 (11.7) 44 (6.0) 20 (2.8) 6 (0.8) 0 (0.0) 0.35 ± 0.78 <0.001Married 221 (%) 115 (52.0) 46 (20.8) 35 (15.8) 22 (10.0) 2 (0.9) 1 (0.5) 0.88 ± 1.11Divorced 7 (%) 7 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0.00 ± 0.00

Ethnic groupLao Loum 811 (%) 581 (71.6) 115 (14.2) 70 (8.6) 39 (4.8) 6 (0.8) 0 (0.0) 0.49 ± 0.89 0.014Lao Soung 56 (%) 44 (78.6) 10 (17.8) 1 (1.8) 0 (0.0) 1 (1.8) 0 (0.0) 0.29 ± 0.68Lao Theung 94 (%) 74 (78.7) 7 (7.4) 8 (8.5) 3 (3.2) 1 (1.1) 1 (1.1) 0.44 ± 0.98

FacultyBasic sciences 143 (%) 124 (86.7) 12 (8.4) 7 (4.9) 0 (0.0) 0 (0.0) 0 (0.0) 0.18 ± 0.50 <0.001Medicine 167 (%) 82 (49.1) 44 (26.4) 26 (15.5) 12 (7.2) 3 (1.8) 0 (0.0) 0.86 ± 1.04Pharmacy 148 (%) 137 (92.6) 10 (6.7) 1 (0.7) 0 (0.0) 0 (0.0) 0 (0.0) 0.08 ± 0.30Dentistry 139 (%) 127 (91.4) 11 (7.9) 1 (0.7) 0 (0.0) 0 (0.0) 0 (0.0) 0.09 ± 0.32Nursing sciences 159 (%) 127 (79.9) 24 (15.1) 5 (3.1) 3 (1.9) 0 (0.0) 0 (0.0) 0.27 ± 0.61Medical technology 99 (%) 89 (89.9) 10 (10.1) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0.10 ± 0.30Post-graduate studies 106 (%) 13 (12.3) 21 (19.8) 39 (36.8) 27 (25.5) 5 (4.7) 1 (0.9) 1.93 ± 1.10

Duration of studyat UHS

<2 years 262 (%) 205 (78.2) 30 (11.5) 15 (5.7) 11 (4.2) 1 (0.4) 0 (0.0) 0.37 ± 0.80 <0.0012–5 years 616 (%) 454 (73.7) 84 (13.6) 49 (8.0) 23 (3.7) 5 (0.8) 1 (0.2) 0.45 ± 0.87>5 years 83 (%) 40 (48.2) 18 (21.7) 15 (18.1) 8 (9.6) 2 (2.4) 0 (0.0) 0.96 ± 1.13

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nternship in family medicine, or preparation of master degree.herefore, they are older students, 93.4% being over 25 years, withhe highest knowledge scores and more aware of the risk of hep-titis B. Yet more than a third of these students, engaged for mostn clinical practice, are not immunized against hepatitis B. The sit-

ation is worse in the faculties of medicine and nursing scienceshere almost three quarters of the students are unvaccinated. It

hows that the increased risk of occupational exposure is not taken

able 5actors associated with the awareness of being at risk for hepatitis B: results of a logistica

Variables Univariate analysis

cOR CI95%

Study year (ref: first year)Sixth year 2.88 [1.73–4.78]

Fifth year 2.23 [1.41–3.53]

Fourth year 1.81 [1.17–2.80]

Third year 1.07 [0.70–1.64]

Second year 1.09 [0.74–1.62]

Age (ref: <20 years)>25 years 2.99 [1.83–4.88]

20–25 years 1.22 [0.77–1.94]

Ethnic group (ref: Lao Loum)Lao Soung 0.54 [0.33–0.88]

Lao Theung 0.69 [0.38–1.23]

Faculty (ref: Medicine)Pharmacy 0.28 [0.17–0.45]

Dentistry 0.29 [0.18–0.47]

Medical technology 0.11 [0.06–0.21]

Post-graduate studies 0.99 [0.61–1.62]

Basic sciences 0.38 [0.24–0.60]

Nursing sciences 0.32 [0.20–0.51]

Marital status (ref: single)Married 1.82 [1.34–2.47]

Divorced

OR: crude odd ratio; CI95%: confidence interval 95%; p: p-value; aOR: adjusted odd ratio.

into account for these inexperienced young adults. A survey con-ducted among medical students in Tehran, Iran, during their secondyear of hospital internship revealed that only a minority of themregularly observed basic safety measures as wearing gloves, notrecapping used needles and proper disposal of sharp objects, but

87.5% had completed the HBV vaccination schedule [10]. Anotherstudy conducted in Turkey among 1491 third- and fourth-yearnursing students showed that 28.1% of them had experienced a

l regression.

Multivariate analysis

p aOR CI95% p

<0.001 3.42 [1.46–7.99] 0.0050.001 2.94 [1.37–6.30] 0.0060.008 2.55 [1.22–5.35] 0.0130.741 0.89 [0.52–1.52] 0.6760.649 0.79 [0.51–1.23] 0.290

<0.001 2.46 [1.32–4.59] 0.0050.394 0.75 [0.42–1.34] 0.333

0.013 0.51 [0.30–0.87] 0.0140.209 0.82 [0.43–1.58] 0.558

<0.001 0.50 [0.28–0.88] 0.016<0.001 0.43 [0.26–0.72] 0.001<0.001 0.25 [0.09–0.64] 0.004

0.9 1.19 [0.51–8.81] 0.687<0.001 0.94 [0.44–2.01] 0.878<0.001 0.63 [0.28–1.39] 0.250

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eedlestick injury and 5.4% a conjunctival exposure to blood, but5.3% were immunized against HBV [11].

The lowest vaccination coverage rates, between 9 and 13%, arehose of Basic Sciences, Medical Technology, Pharmacy and Den-istry Faculties. For students of Basic sciences, this may be becausehey are younger and not yet exposed to occupational risk of infec-ion with blood-borne viruses. However, in the Faculty of Medicalechnology, Laboratory Students are those who face the greatestisk of hepatitis B. By comparison, in a study conducted in Newelhi, India, on a whole microbiology laboratory staff, 47.3% of thearticipants were completely vaccinated, 20.8% were partially vac-inated and 31.9% were not vaccinated at all [12]. Finally, less than0% of dental students are properly immunized whereas they willxercise one of the professions most at risk for hepatitis B. A sur-ey conducted among 112 students from three dental schools inigeria revealed that 50.9% of them reported one or more occupa-

ional exposure to body fluids during the previous six months, butnly 36.6% were immunized against hepatitis B [13]. Although theiterature shows that HCWs are inadequately protected against theisk of HBV infection in most countries of the world, immunizationoverage rates observed in our study are among the lowest evereported.

How to explain such low vaccination coverage against hepatitis among these students already or soon to be exposed to occupa-ional risks of contamination?

The first reason is the lack of knowledge about hepatitis B, morehan 72% of students surveyed are unable to meet one of the fivepen-ended questions about hepatitis B and 98% are unaware of theisk factors of HBV infection. Similar surveys got better results using

multiple-choice questionnaire (MCQ). A cross-sectional surveyonducted in 14 nursing schools in Turkey found an average score of0.8 out of 14 questions with a questionnaire on hepatitis B callingor answers such as “yes – no – do not know” [11]. Another surveyf the same design, conducted with a MCQ among 242 studentsf medical sciences university in Iran, found an average level ofnowledge of 17 ± 5 from 28 questions [14]. It is easier to get aood score with close-ended questionnaires than with open-endednes because MCQs may influence students in their response, whileriting requires not only to remember the correct answer but also

o use higher cognitive skills [15]. The fact remains that the level ofnowledge is very poor, more than a quarter of the students havingever heard of hepatitis B, while hepatitis B is theoretically included

n the educational programme of each of the seven faculties of UHS,n the fourth year for the medical students.

Moreover, even where the HCWs have a high level of risk aware-ess, their personal protection is not guaranteed. A study in Nigeriamong operating room staff revealed a poor immunization status26.8%) despite a good knowledge of risk factors for hepatitis B andaccine against HBV [16]. The lack of motivation of students to beaccinated against hepatitis B appears to be related to a poor per-eption of occupational risk of contamination, but also to a certainarelessness as their main excuse is not knowing where to get vac-inated. The second reason cited by 15.7% of unvaccinated students,as that the vaccine is too expensive. Such explanation is difficult

o accept in a country undergoing economic transition where therice of one dose of hepatitis B vaccine is only 50,000 LAK (about.25 U.S. dollars).

Are students of UHS, born and living in highly endemic countries,till at risk for HBV infection in adulthood? The relevance of uni-ersal hepatitis B vaccination of HCWs has been questioned in aniversity hospital in Niger where 92% of the staff was HBcAg pos-

tive. With such a small proportion of susceptible people to HBV

nfection, priority should be given to prevention of bloodborneathogens transmission by struggling against accidental exposureo blood, these measures being effective against HBV, but also HCVnd HIV [17]. Our survey did not include serological testing for HBV

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infection. A routine pre-vaccination screening by anti-HBc testing,performed in Laos for 80,000 LAK (about 10 U.S. dollars), could becost-effective if the prevalence of this marker in the student pop-ulation was over 50% [18]. However, a recent study conducted inVientiane among 906 blood donors shows that 45% of donors 20–29years aged were anti-HBc positive [19]. Waiting a serosurvey tospecify the prevalence of HBV infection markers among UHS stu-dents, the available data argue in favour of a routine vaccinationwithout screening.

Although this is a major target, the national strategy against hep-atitis B should not be limited to the prevention of mother-to-childtransmission. It must integrate a policy of prevention of bloodbornepathogens in HCWs early in their training. Upon their admission tothe UHS, all students should receive theoretical and practical infor-mation to avoid accidental exposure to blood and be vaccinatedagainst hepatitis B.

Acknowledgments

This study was funded by the Agence Universitaire de laFrancophonie (AUF) and the Institut de la Francophonie pour laMédecine Tropicale (IFMT) (grant number Budget AUF/IFMT 2013).We express our gratitude to the Rector and Deans of the Univer-sity of Health Sciences of Laos for their help in carrying out ourinvestigation.

Authors’ contributions: KP, PK, FQ, VL and YB contributed to thestudy design; KP and PK conducted the entire investigation; KP, PK,FQ and VS performed the statistical analysis; VL, VS and YB gatheredvaluable information on University of Health Sciences and helpedto develop the recommendations. All authors read and approvedthe final manuscript. Conflict of interest: The authors declare thatthey have no competing interest.

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