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Journal of Infection and Public Health 11 (2018) 89–93

Contents lists available at ScienceDirect

Journal of Infection and Public Health

j o u r n a l h o m e p a g e : h t t p : / / w w w . e l s e v i e r . c o m / l o c a t e / j i p h

ERS-CoV infection: Mind the public knowledge gap

men Bawazir a,∗, Eman Al-Mazroo b, Hoda Jradi a, Anwar Ahmed a, Motasim Badri a

College of Public Health and Health Informatics1 , King Saud Bin Abdulaziz University for Health Sciences2 , Saudi Arabia Infection Control Department, Ministry of National Guard Health Affairs, Riyadh, Saudi Arabia

r t i c l e i n f o

rticle history: eceived 31 January 2017 eceived in revised form 5 April 2017 ccepted 1 May 2017

eywords: orona virus ttitude iyadh audi Arabia ERS-CoV

a b s t r a c t

In August 2015, the Corona outbreak caused by Middle East respiratory syndrome coronavirus (MERS- CoV) was the 9th episode since June 2012 in Saudi Arabia. Little is known about the public awareness toward the nature or prevention of the disease. The aim of this work was to assess the knowledge of the adult population in Riyadh toward the MERS-CoV.

In this cross-sectional survey, a self-administrated questionnaire was distributed to randomly selected participants visiting malls in Riyadh. The questionnaire contained measurable epidemiological and clin- ical MERS-CoV knowledge level variables and relevant source of information.

The study included 676 participants. Mean age was 32.5 (±SD 8.6) years and 353 (47.8%) were males. Almost all participants heard about the corona disease and causative agent. The study showed a fair overall knowledge (66.0%), less knowledge on epidemiological features of the disease (58.3%), and good knowledge (90.7%) on the clinical manifestation of the MERS-CoV. Internet was the major (89.0%) source of disease information, and other sources including health care providers, SMS, television, magazines and books were low rated (all <25%). In a multivariate logistic regression analysis age ≤30 years (Odds Ratio (OR) = 1.647, 95%CI 1.048–2.584, P = 0.030), male gender (OR = 1.536, 95%CI 1.105–2.134, P = 0.01), and no tertiary education (OR = 1.957, 95%CI 1.264–3.030, P = 0.003) were independent significant predictors of poor epidemiological knowledge.

This study concludes that there was inadequate epidemiological knowledge received by the public and the reliance mostly on the clinical manifestations to recognizing the MERS-CoV disease. Compre- hensive public health education programs is important to increase awareness of simple epidemiological determinants of the disease is warranted.

© 2017 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health Sciences. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/

ntroduction

Middle East respiratory syndrome coronavirus (MERS-CoV) is a ovel coronavirus that causes a viral respiratory disease (Middle ast respiratory syndrome, MERS) [1]. Globally, the World Health rganization (WHO) has reported 1864 laboratory-confirmed

ERS-CoV cases with 659 associated deaths in 27 countries since

eptember 2012 [2]. According to the last WHO report, the King- om of Saudi Arabia (KSA) remains the most afflicted country,

∗ Corresponding author at: Department of Community and Environmental Health, ollege of Public Health and Health Informatics, King Saud Bin Abdulaziz University

or Health Sciences, King Abdulaziz Medical City, National Guard Health Affairs, Mail ode 2350, P.O. Box 3660, Riyadh 11481, Saudi Arabia.

E-mail addresses: [email protected], [email protected] A. Bawazir).

1 http://cphhi.ksau-hs.edu.sa. 2 www.ksau-hs.edu.sa.

ttps://doi.org/10.1016/j.jiph.2017.05.003 876-0341/© 2017 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz Un

icense (http://creativecommons.org/licenses/by-nc-nd/4.0/).

licenses/by-nc-nd/4.0/).

with remarkable morbidity and mortality rates [3]. The first case of coronavirus infection was identified in the KSA in June 2012 [4]. Subsequently, continuous detection of the virus has been reported in different healthcare facilities in the KSA and other Asian coun- tries, including Korea, the United Arab Emirates and Iran [5–8]. Most of the reported cases have emerged from the Middle East; other cases reported elsewhere had direct connections with pri- mary cases of infection in the Middle East [9]. Therefore, many countries worldwide have implemented prevention measures, par- ticularly amongst potential travelers to Middle Eastern countries. The KSA is a particular concern since it is the epicenter of the dis- ease and a destination for millions seeking the Haj pilgrimage or Umrah annually.

Strict guidelines have been developed for disease control and

prevention, with a particular emphasis on protective measures [10]. These guidelines include frequent and thorough hand wash- ing and avoiding people who are sick and coughing, undercooked meat, unsafe water, close contact with animals and camel-based

iversity for Health Sciences. This is an open access article under the CC BY-NC-ND

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0 A. Bawazir et al. / Journal of Infect

roducts, such unpasteurized milk or raw meat [4]. Because no ERS-CoV vaccine is available currently, these protective measures

an potentially reduce the risk of viral infection. Major gaps exist in the knowledge of the epidemiology, preva-

ence and clinical spectrum of the infection [1]. As highlighted by he WHO, provision of information to the general public about the irus, its transmission modes and adequate protective measures is he cornerstone for prevention and control of the disease [10,11].

Although there is a great need to clarify the nature, genomic eatures, and epidemiological characteristics of the disease, the umber of investigations conducted in this field is far from the xpected. This information is urgently needed for the planning nd effective implementation of preventive and control measures o combat dissemination of the virus within and outside of the

iddle Eastern region. Despite the strong link between the trans- ission patterns of the disease and both zoonotic transfers and

uman-to-human transmission [12], data on the risk and contribut- ng factors to the rapid spread and health effects of the virus are acking, particularly in hospitalized patients from the KSA [8]. Sig- ificant questions remain unanswered on the extent of the Saudi eople’s awareness of the characteristics and nature of this virus. inding answers to these questions is instrumental for the imple- entation of effective preventive measures to reduce and control

he frequent occurrence of MERS-CoV outbreaks. Increased public wareness of the disease may decrease the risk of the virus and elp combat the disease in the annual mass-gathering events that ccur in the KSA, such as the Hajj and Umrah. This study aimed o identify the gap in knowledge of the adult population resid- ng in Riyadh, KSA, toward the nature and transmission modes of

ERS-CoV infection.

ethods

A cross-sectional study was conducted from June to September f 2015. Five main commercial malls in Riyadh were randomly elected. People in the main cities in the KSA visit malls for dif- erent purposes, including shopping and entertainment, all year ong. Therefore, malls can be considered representative of the Saudi opulation for purposes such as scientific research. Approval for he project was obtained from the Research Committee, College f Public Health and Health Informatics, King Saud Bin Abdul-Aziz niversity for Health Sciences, and from the Institutional Research oard Committee (IRBC) at King Abdullah International Medical esearch Center (KAIMRC) (#IRBC/383/15), Riyadh, National Guard ealth Affairs at the Ministry of the National Guard.

The study included Saudi adults living in Riyadh aged 18 years nd older. The study excluded non-Saudi adults or visitors from utside of Riyadh. Proportional quota sampling was used to ensure hat the respondents were demographically representative of the eneral population, with quotas based on age, gender, region and ocial class. A sample size of 768 was calculated based on an xpected 50% proportion of poor knowledge in this population oward MERS-CoV transmission and prevention measures at 80% ower with a 95% confidence level and a design effect of two [10].

two-stage sampling method was employed. The first stage con- isted of selecting 5 top malls located in different zones of Riyadh ity (north, south, middle, east, and west). Then, a simple random ample of adults shopping in these malls who were willing to par- icipate in the study was interviewed using a self-administered uestionnaire. To measure the level of knowledge in both males and emales, a 1:1 ratio was purposefully chosen. The enrollment strat-

gy was undertaken to cover all three different work shifts of the alls (morning, afternoon, and night). Of 768 possible participants,

76 individuals of both genders were successfully interviewed response rate = 88.02%).

d Public Health 11 (2018) 89–93

Data collection tool

All respondents were informed of the purpose of the study. Con- senting participants were selected randomly from each study site, and a self-administered questionnaire was distributed and filled out by the participants. The questionnaire was initially designed in English after a thorough search for relevant recent literature on public knowledge, attitudes and practices. Further information was retrieved from the WHO and the KSA Ministry of Health websites on both the H1N1 virus [10] and MERS-CoV [13–15] and was adapted with some modifications to the local context of both the nature of coronaviruses and the cultural context of the KSA. Furthermore, the questionnaire was reviewed by experts in infectious diseases for relevance, simplicity and internal consistency. Arabic translation of the questionnaire was conducted by a professional translator.

The questionnaire was designed to contain 5 parts, of which three parts were reported in this study. These parts included socio- demographic information [age (<30 or ≥30 years), gender, marital status (married or unmarried), education level (tertiary or no ter- tiary) and occupation (employed or unemployed)], seven questions on the participants’ sources of information about the disease and 18 questions measuring the level of knowledge (nature of the disease, transmission, signs and symptoms, and methods of prevention). A Likert scale (yes, no, and do not know) was used in 18 questions to measure knowledge. The 18 knowledge questions were catego- rized into two knowledge domains (epidemiological and clinical). The former domain included 10 questions, and the latter domain included 8 questions. The epidemiological domain questions were related to knowledge of the nature of the causative agent, modes of transmission (droplets, contact, and animal to man or other trans- mission), incubation period and availability of vaccines. The clinical domain measured knowledge of the clinical signs and symptoms (cough, fever, shortness of breath, pharyngitis, diarrhea, no symp- toms, death and other consequences) and questions inquiring about the availability of a cure for the disease. To evaluate the responses to these questions, a correct answer was allocated a value of one, and a wrong answer was allocated a value of zero. The total possi- ble knowledge score of 18 (range from 0 to 18) was dichotomized to poor knowledge if the total score was <14 (25th percentile of the total score) or good knowledge if the score was ≥14.

A pilot study on 20 subjects was conducted, and the data were analyzed to ensure face validity, comprehension and feasibility. Cronbach’s alpha reliability coefficient was 0.71, which was con- sidered satisfactory for the purpose of this study.

Data analysis

Data were summarized as frequencies and proportions and were compared using the Chi-square test. Logistic regression models were fitted to identify factors associated with a poor score (a score <14). Variables found significant in the univariate analyses were included in the final multivariate logistic regression analysis. All tests were two-sided, and statistical significance was considered at a P-value of <0.05. The data entry and statistical analysis were per- formed using the Statistical Program for Social Sciences (IBM SPSS Corp, SPSS Statistics ver. 20, USA).

Results

Sociodemographic characteristics of the participants

The study included 676 participants. Of these, 289 (42.8%) were aged <30 years, 353 (52.2%) were males, 389 (57.5%) were mar- ried, 557 (82.4%) had received a tertiary education and 622 (92%)

A. Bawazir et al. / Journal of Infection an

Table 1 Socio-demographic characteristics of the participants (N = 676).

Characteristics n %

Age >30 years 289 42.8 ≤30 years 387 57.2

Gender Female 323 47.8 Male 353 52.2

Marital status Married 389 57.5 Unmarried 287 42.5

Tertiary education No 119 17.6 Yes 557 82.4

Employment No 54 8.0 Yes 622 92.0

Table 2 Association between source of information and overall level of knowledge on MERS- CoV.

Poor High Total

No. % No. % No. % P-value

Internet 257 87.1 539 90.0 796 89.0 0.197 SMS 80 27.1 134 22.4 214 23.9 0.118 Television 52 17.6 115 19.2 167 18.7 0.571 Health care workers 40 13.6 99 16.5 139 15.5 0.249

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Family members 34 11.5 79 13.2 113 12.6 0.482 Magazines 29 9.8 69 11.5 98 11.0 0.447 Books 19 6.4 55 9.2 74 8.3 0.162

ere employed. The sociodemographic characteristics of the par- icipants are shown in Table 1.

ource of information regarding the disease

The majority (89.0%) of the respondents reported that informa- ion about MERS-CoV was received from the internet, followed by he SMS (23.9%). Few participants reported that they received infor-

ation from other sources, such as television, healthcare workers, amily members, magazines or books (18.7%, 15.5%, 12.6%, 11.0%, nd 8.3%, respectively). No significant differences were found in he sources of information between respondents with a good or oor level of knowledge on MERS-CoV in this cohort of participants Table 2).

nowledge assessment

Table 3 shows the frequencies of correct responses to each ques- ion in the epidemiological and clinical domains. Almost all of the articipants had heard of the coronavirus disease and were able

able 3 ositive responses on different questions related to epidemiological and clinical knowled

Questions

1 Have you ever heard about Corona (MERS-CoV) 2 The corona disease is caused by a virus 3 MERS-CoV can be transmitted through cough droplets 4 MERS-CoV can be transmitted from person to person 5 MERS-CoV can be transmitted through talk with others 6 MERS-CoV can be transmitted through hand shake with ot 7 MERS-CoV can be transmitted from animal to person 8 Camels transmit the virus 9 MERS-CoV can cause multiple infections 10 Do you know of a vaccine against MERS-CoV 11 Fever and cough are among the signs and symptoms of ME 12 Shortness of breath is among the signs and symptoms of M 13 Pharyngitis is among the signs and symptoms of MERS-CoV 14 Diarrhea is among the signs and symptoms of MERS-CoV 15 MERS-CoV can lead to direct death 16 Do you know how long after exposure to MERS-CoV can an 17 A MERS-CoV patient can be cured 18 MERS-CoV can be found in individuals with no signs or sym

d Public Health 11 (2018) 89–93 91

to relate its cause to a viral origin (100% and 99%, respectively). The participants also highly recognized the mode of transmis- sion of the disease as via the respiratory tract through coughing (99.0%) and from person to person (94.4%). However, they were less likely to associate the transmission of infection with talking with an infected person or to shaking hands with an infected per- son (52.4% and 49.3%, respectively). Frequencies of correct answers to questions related to whether the virus could be transmitted from an animal to a person, whether the camel was a reservoir of the causative agent, whether the agent could cause repeated infections and whether they knew of any vaccine against the agent were 86.4%, 84.8%, 66.3%, and 75.1%, respectively. Knowl- edge about signs and symptoms, such as fever, cough, shortness of breath, pharyngitis and diarrhea, was high (97%). Questions such as “Could MERS-CoV lead to direct death” also showed a high rate of positive answers (89.5%). However, the participants’ knowledge about other questions related to the incubation period of the disease, the recovery of patients and infection without signs and symptoms was poor (59.2%, 25.0%, and 24.1%, respec- tively).

Factors related to knowledge about MERS-CoV

Overall, good knowledge was reported in this study (66.4%). However, according to the analysis of the two knowledge domains (epidemiological and clinical), the participants were less knowl- edgeable (58.3%) regarding the epidemiological features of the disease, whereas they scored high in knowledge (90.7%) regarding the clinical manifestation of MERS-CoV (Table 4).

The overall level of knowledge varied across several charac- teristics of the study participants. Individuals who were 30 years of age or older (P = 0.016), female (P = 0.04), married (P = 0.028), had received a tertiary education (P < 0.001) and were employed (P = 0.10) showed significantly better overall knowledge about MERS-CoV than their counterparts. Knowledge about the clini- cal manifestations of the disease did not vary significantly by age (P = 0.58), marital status (P = 0.54), or employment status (P = 0.34) (Table 4).

Table 5 shows the final multivariate logistic models for inde- pendent predictors of poor epidemiological, clinical, and overall knowledge scores. Some socio-demographic characteristics, such

as age, gender, and education level, were significant independent predictors of poor epidemiological knowledge, whereas only the female gender and a tertiary educational level were significant pre- dictors for poor clinical knowledge (Table 5).

ge.

n %

676 100.0 669 99.0 672 99.4 638 94.4 354 52.4

hers 333 49.3 584 86.4 573 84.8 448 66.3 508 75.1

RS-CoV 670 99.1 ERS-CoV 668 98.8

669 99.0 662 97.7 605 89.5

individual get sick 400 59.2 169 25.0

ptoms 163 24.1

92 A. Bawazir et al. / Journal of Infection and Public Health 11 (2018) 89–93

Table 4 Association between participant characteristics and epidemiological, clinical and overall knowledge toward MERS-CoV disease.

Epidemiological Clinical Overall

Characteristic Good Poor Good Poor Good Poor

n % n % P† n % n % P n % n % P

Age >30 years 152 38.6 137 48.6 0.010 260 42.4 29 46.0 0.580 176 39.5 113 49.1 0.016 ≤30 years 242 61.4 145 51.4 353 57.6 34 54.0 270 60.5 117 50.9

Gender Female 202 51.3 121 42.9 0.032 305 49.8 18 28.6 0.001 231 51.8 92 40.0 0.004 Male 192 48.7 161 57.1 308 50.2 45 71.4 215 48.2 138 60.0

Marital status Married 240 60.9 149 52.8 0.036 355 57.9 34 54.0 0.546 270 60.5 119 51.7 0.028 Unmarried 154 39.1 133 47.2 258 42.1 29 46.0 176 39.5 111 48.3

University No 49 12.4 70 24.8 0.000 93 15.2 26 41.3 0.000 55 12.3 64 27.8 0.000 Yes 345 87.6 212 75.2 520 84.8 37 58.7 391 87.7 166 72.2

Employment No 24 6.1 30 10.6 0.032 47 7.7 7 11.1 0.337 27 6.1 27 11.7 0.010 Yes 370 93.9 252 89.4 566 92.3 56 88.9 419 93.9 203 88.3

P†: � test.

Table 5 Multivariate factors associated with the poor knowledge toward MERS-CoV disease.

Epidemiological Clinical Overall

Factor OR† 95% CI P‡ OR 95% CI P OR 95% CI P

Age (years) >30 years 1.647 1.048–2.584 0.030 1.370 0.660–2.950 0.421 1.618 1.01–2.591 0.045 ≤30 years 1 1 1

Gender Male 1.536 1.105–2.134 0.011 2.556 1.399–4.670 0.002 1.790 1.264–2.534 <0.001 Female 1 1 1

Marital status Unmarried 0.845 0.538–1.328 0.466 0.640 0.294–1.395 0.262 0.846 0.528–1.356 0.487 Married 1 1 1

University No University 1.957 1.264–3.030 0.003 4.059 2.196–7.502 <0.0001 2.267 1.460–3.520 <0.001 University 1 1 1

1.0 1

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k u h q s e H h n f e o k n a t p d h a a t d t R e a a n u

Employment Employed 1.576 0.855–2.904 0.145 Unemployed 1

R†: Odds ratio. P‡ Wald test.

iscussion

The present study measured epidemiological and clinical nowledge regarding the MERS-CoV disease among the Saudi pop- lation in Riyadh city. Approximately 66% of the study participants ad overall good knowledge regarding MERS-CoV (66.4%). This fre- uency is comparable to the reported knowledge score from a tudy conducted in Al Qaseem (73.2%) but higher than the knowl- dge score reported in a study conducted in Makah (32.4%) [15,16]. owever, these two studies enrolled only healthcare workers and ad different sample sizes and respondent characteristics. More urses were included in the study from Makah than in the study

rom Qaseem. Our study went further to explore the gap in knowl- dge among the general population regarding the characteristics f the disease and to determine related factors. To the best of our nowledge, this study is the first to comprehensively assess the ecessary and required epidemiological and clinical knowledge spects of the disease. The study highlights gaps in knowledge and he essential elements required to educate and encourage the Saudi ublic to play active roles in the prevention and treatment of the isease and possibly reverse the course of this rapidly growing, ighly infectious and fatal disease. Additionally, our study adopted

unique approach of separately evaluating the epidemiological nd clinical knowledge domains, which typically are combined ogether in similar studies. Combined assessment of these two omains might overstate the overall knowledge score and obscure he identification of areas with a significant lack of knowledge. eliance mostly on the clinical manifestations of these types of dis- ases to assess public knowledge might produce biased results. Our

pproach allowed us to glean information concerning these areas nd identify inadequate epidemiological knowledge and skills that eed urgent educational interventions. This approach could be seful for similar studies evaluating public knowledge toward

26 0.402–2.617 0.957 1.742 0.938–3.235 0.079 1

infectious diseases other than Mers-Cov, such SARS, H1N1, Zika, and Ebola.

The overall aim of our analysis was to determine whether the epidemiological and clinical features of the disease were well understood by the public. The findings demonstrated that the pub- lic was less knowledgeable regarding the epidemiological features of the disease (58.3%), whereas they expressed good knowledge (90.7%) on the clinical aspects of the disease. In a recent study conducted in Riyadh, Al-Mutairi et al. reported a high rate (91.6%) of public awareness of the viral cause of MERS-CoV [17]. Almu- tairi et al. relied exclusively on the clinical manifestations of the MERS-CoV disease in their assessment of public knowledge. Com- pared with the Almutairi et al., study, our study adopted a unique approach of separately evaluating the epidemiological and clinical knowledge domains.

Al-Mohrej and his colleagues concluded in a similar study that Saudi public awareness of MERS-CoV was generally satisfactory [18]. A previous study conducted among the Saudi public in Riyadh regarding the swine flu demonstrated that only 56% of the pop- ulation was knowledgeable of this viral diseases [19]. This issue of insufficient knowledge of the Saudi public regarding frequently emerging outbreaks underscores the level of implementation of public preventive measures related to outbreak control. Many pre- vious studies designed to assess public attitudes and knowledge regarding the nature of diseases causing outbreaks, such as SARS, H1N1 influenza, and recently MERS-CoV, found that the majority of the participants lacked appropriate information about the infec- tious agents and how to behave adequately toward these infections [7,9,12,20–23].

The significant predictors of the participants’ overall good knowledge in our study were an age ≥30 years, a university edu- cational level, and female gender. This pattern suggests that more emphasis should be placed on the young, male participants and

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[ Avian influenza risk perception, Europe and Asia. Emerg Infect Diseases 2007;13(2):290.

[24] Hoda J. Identification of information types and sources by the public for pro- moting awareness of Middle East respiratory syndrome coronavirus in Saudi Arabia. Health Educ Res 2016;31(1):12–23.

A. Bawazir et al. / Journal of Infect

hose with a low level of education in programs aimed at increas- ng awareness of the disease among the public to improve their nowledge about the pandemic MERS-CoV disease.

Similar to a recent study regarding information-seeking behav- or for MERS-CoV in Saudi Arabia [24], most of the participants in his study reported the Internet as their main source of information bout MERS-CoV. For this particular reason, research is urgently eeded to determine how the Internet can be used for health pro- otion, particularly for emerging infectious diseases in this country

r in a similar context. Alarmingly, the previous study found that he individuals who underestimated the fatality rate of MERS-CoV isease received their information from the Internet [24]. This find-

ng may suggest that the quality of information currently available hrough the Internet is inadequate and in need of revision. More- ver, a very low percentage of participants indicated that their ain source of information was healthcare providers. This scenario

eflects a lack of engagement of healthcare workers in increasing wareness of the public regarding the different aspects of MERS- oV. Measures should be taken to ensure that healthcare workers ctually assume their role as the main providers of reliable and orrect information.

We acknowledge our study limitations. The study was based n a self-reported questionnaire. Therefore, recall bias and social esirability bias cannot be excluded. The impact of these biases in ur study is difficult to assess. The inclusion of innovative interven- ional methods with informative evaluation plans to monitor the evel of knowledge among the community, respond to their needs nd fill the gaps with better preventive methods would be helpful n prospective research.

onclusion

Promotion of public knowledge, attitudes and behaviors toward ERS-CoV disease is important due to the virulence, high fatality

ate and risk of rapid transmission of the virus in the community. ndividuals need more information about the MERS-CoV disease, ts transmission mode, and the preventive measures required to

inimize its impact. Government health systems and institutions hould design and implement advanced and motivational health romotion programs to educate the public and healthcare work- rs about infectious diseases in general that may spread among opulations and about all possible future pandemics.

uthors’ contribution

The study was conceptualized and designed by AB. The data ere collected by EA. The data analysis was conducted by AB, AA

nd MB. The manuscript was drafted by AB and HJ. All authors crit- cally reviewed and approved the final version of the manuscript.

unding

No funding sources.

ompeting interests

None declared.

thical approval

KAIMRC # IRBC/383/15.

d Public Health 11 (2018) 89–93 93

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