Eastern Mediterranean La Revue de Santé de Health Journal la Méditerranée orientale

املجلد الثاين و العرشون عدد Vol. 22 No. 10 • 2016 • 10 Contents

Editorial Sustainable Development Agenda 2030 thrives on health Z. Mirza...... 711 Research articles Iranian public trust in health services: evidence from Tabriz, Islamic Republic of Iran J.S. Tabrizi, M. Saadati, H. Sadeghi-Bazargani, L. Abedi and R. Alibabayee...... 713 Tobacco chewing and risk of gastric cancer: a case–control study in Yemen F.A. Al-qadasi, S.A. Shah, H.F. Ghazi...... 719 Job satisfaction and its relationship to Radiation Protection Knowledge, Attitude and Practice (RP-KAP) of Iranian radiation workers S.S. Alavi, S.T. Dabbagh, M. Abbasi and R. Mehrdad...... 727 Turkish version of the SPAN questionnaire for high-school students: reproducibility and validity F. Öz, S. Metintas, R. Aydın and Ö. Özay...... 735 Knowledge of diabetes among patients in the United Arab and trends since 2001: a study using the Michigan Diabetes Knowledge Test M. Jawad Hashim, H. Mustafa and H. Ali...... 742 Preliminary estimates of the economic implications of addiction in the C.M. Doran...... 749 Prevalence and seasonal variation of human intestinal parasites in patients attending hospital with abdominal symptoms in northern Jordan A.S. Jaran...... 756 Report Overview of the 63rd session of the WHO Regional Committee for the Eastern Mediterranean Ala Alwan...... 761 Review Dietary transition and obesity in selected Arabic-speaking countries: a review of the current evidence B.H. Aboul-Enein, J. Bernstein and A.C. Neary...... 763 WHO events addressing public health priorities Intercountry meeting on controlled medicines...... 771 Ala Alwan, Editor-in-chief Editorial Board Zulfiqar Bhutta Mahmoud Fahmy Fathalla Rita Giacaman Ahmed Mandil Ziad Memish Arash Rashidian Sameen Siddiqi Huda Zurayk International Advisory Panel Mansour M. Al-Nozha Fereidoun Azizi Rafik Boukhris Majid Ezzati Hans V. Hogerzeil Mohamed A. Ghoneim Alan Lopez Hossein Malekafzali El-Sheikh Mahgoub Hooman Momen Sania Nishtar Hikmat Shaarbaf Salman Rawaf Editors Phillip Dingwall Guy Penet (French) Eva Abdin, Fiona Curlet, Cathel Kerr, Marie-France Roux (Freelance) Manar Abdel-Rahman, Ahmed Bahnassy, Abbas Rahimiforoushani (Statistics) Graphics Suhaib Al Asbahi, Diana Tawadros Administration Nadia Abu-Saleh, Yasmeen Sedky, Iman Fawzy

Cover designed by Diana Tawadros Internal layout designed by Emad Marji and Diana Tawadros Printed by WHO Regional Office for the Eastern Mediterranean Cover photograph ©World Health Organization املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Editorial Sustainable Development Agenda 2030 thrives on health Z. Mirza 1

Never before has the flight of human current health issues, including the Never before had such a bold ambition imagination made calls for universal need to strengthen health systems. embraced the aspirations of all citizens development that are so loud and Target SDG3.8 is bold in terms of sharing the planet, given that the Reso- audacious. The all-encompassing Sus- its scope, namely “achieve universal lution mandated for all United Nations tainable Development Agenda 2030 health coverage, including financial (UN) members take action on this (SD Agenda 2030) has evolved over risk protection, access to quality es- Agenda. Clearly such an array of goals 67 years since the adoption of the Uni- sential health-care services and ac- is not within the competencies and versal Declaration of Human Rights by cess to safe, effective, quality and bounds of a single agency; thus, inter- the United Nations in 1948. Although affordable essential medicines and sectoral action and partnerships were based on the same principle of univer- vaccines for all” (4). made part of the agenda itself, resulting sality, the scope of the Agenda is much The interdependence of SDGs in the 17th SDG, titled “Strengthen broader. It is a melting-pot of human is highlighted through SDG3 and its the means of implementation and rights, environmental movements and relationship with the other 16 SDGs, revitalize the Global Partnership for the fight against poverty; hence, it is a which are: poverty, hunger, educa- Sustainable Development” (4). In plan of action for people, the planet and tion, gender equality, water and sani- addition, an elaborate framework of prosperity. Moreover, it also seeks peace tation, energy, economic growth, 230 indicators has been developed by as a necessary condition for develop- inclusive and sustainable industri- the Inter-Agency and Expert Group ment. alization and innovation, inequality, (IAEG) on SDG Indicators to moni- The symbiotic relationship be- safe cities, sustainable consumption tor progress in implementation of this tween health and development is well and production, climate change, action plan for global transformation understood. The historic Alma-Ata sustainable use of water reservoirs, (5). Totaling 26 indicators, the health Declaration on Primary Health Care environmental protection, peace goal has the largest number of proposed in 1978 (1) and the work of the WHO and justice, and partnerships. Health indicators of all 17 SDGs. Unlike Mil- Commission on Social Determinants will benefit from development in lennium Development Goals (MDGs), of Health (2) have unequivocally estab- each of these areas, just as health which constituted a less focused agenda lished that for health to be attained there also contributes to the advancement and was mainly donor driven (despite is a need for “action of many other social towards these goals. For example, some remarkable achievements), the and economic sectors in addition to when poverty is reduced there are SD Agenda 2030 is the responsibility of the health sector” (1). The more recent fewer incidences of poverty-related Member States. work on health-in-all-policies approach diseases, and citizens are able to What does the SD Agenda 2030 (3) is also embedded in the importance spend more on their health. Thus, mean to governments and develop- of inter-sectoral action to protect and healthy individuals are able to work ment partners, and how can they work promote health. more, earn better wages and enjoy in partnership to support it? This is the The centrality of health in the SD economic prosperity. Such health important question being addressed Agenda 2030 is evident through the benefit–contribution relationships by both sides. The comprehensive na- links that the Sustainable Development exist for all other goals. ture of the Agenda is such that either Goal 3 (SDG3) has with the remain- On 25 September 2015, the national development planning com- ing 16 SDGs. SDG3 aims to “Ensure General Assembly of United Nations missions/ministries, or their equivalent healthy lives and promote well-being adopted Resolution 70/1 titled “Trans- pivotal bodies, have to take on the lead- for all at all ages” (4) and its 13 tar- forming Our World: the 2030 Agenda ership role and coordinate, or this work gets cover practically all aspects of for Sustainable Development” (4). must be led by the prime ministerial/

1Director, Health System Development (HSD), WHO Regional Office for the Eastern Mediterranean, Cairo, Egypt

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presidential offices. Likewise, develop- visions have to align with SDGs. World WHO’s work, and has implications ment partners must also break their Health Organization (WHO) is lead- for priorities and working practices “silo” approach and work at an intera- ing on SDG3 and actively developing throughout the Organization. How the gency level. SD Agenda 2030 requires a the required institutional arrangements current generation of development prac- holistic governmental approach, which for this substantial undertaking. titioners lived up to achieving the grand demands financing and strong leader- Thus, the SDG agenda remains a mission agreed in September 2015 will ship, whereby national development major driving force behind much of be judged by future generations.

References

1. Declaration of Alma-Ata. International Conference on Primary ing policies. Helsinki: Ministry of Social Affairs and Health, Health Care. Alma-Ata, USSR, 6–12 September, 1978 (http:// Finland; 2013 (http://www.euro.who.int/__data/assets/ www.who.int/publications/almaata_declaration_en.pdf). pdf_file/0007/188809/Health-in-All-Policies-final.pdf). 2. Commission on Social Determinants of Health (CSDH). Clos- 4. Resolution A/RES/70/1. Transforming our world: the 2030 ing the gap in a generation: health equity through action on agenda for sustainable development. United Nations General the social determinants of health. Final Report of the Com- Assembly 70th session; New York: United Nations; 25 Septem- mission on Social Determinants of Health. Geneva: World ber 2015 (https://sustainabledevelopment.un.org/post2015/ Health Organization; 2008 (http://apps.who.int/iris/bitstre transformingourworld) am/10665/43943/1/9789241563703_eng.pdf). 5. Sustainable Development Goal indicators. New York: United 3. European Observatory on Health Systems and Policies. Nations Statistics Division (http://unstats.un.org/sdgs/). Health in all policies, seizing opportunities, implement-

712 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Iranian public trust in health services: evidence from Tabriz, Islamic Republic of Iran J.S. Tabrizi 1, M. Saadati 2, H. Sadeghi-Bazargani 3, L. Abedi 4 and R. Alibabayee 5

ثقة اجلمهور باخلدمات الصحية يف تربيز بجمهورية إيران اإلسالمية جعفر صادق تربيزي، حممد سعاديت، مهايون صادقي- بازركاين، ليىل عابدي، رقية عيل بابائي اخلالصــة: لقــد اســتقصت هــذه الدراســة ثقــة اجلمهــور باخلدمــات الصحيــة يف تربيــز بجمهوريــة إيــران اإلســامية. حيــث أجريــت دراســة 1050 2014 أ َرس ّيــة مقطعيــة يف عــام ، ُاســتخدم فيهــا اختبــار العينــة العنقــودي العشــوائي. وقــد ُس ِّــجل يف الدراســة مــا جمموعــه أرسة، ُواســتخدم اســتبيان ذو مصدوقيــة جلمــع البيانــات عــن طريــق إجــراء مقابــات. فــكان متوســط الدرجــات املحــرزة بخصــوص ثقــة اجلمهــور باخلدمــات الصحيــة يف تربيــز 53.91 ± 13.7 )مــن كل 100(. وقــد منــح النــاس أعــىل درجــات الثقــة للخــربة املهنيــة وأدنــى الدرجــات لسياســات الصعيــد الــكيل. وكان االختصاصيــون ودكاتــرة الصيدلــة واملمرضــات مقدمــي الرعايــة الصحيــة الذيــن متتعــوا بأعــىل مســتويات الثقــة. يســتنتج مــن ذلــك أن ثقــة اجلمهــور باخلدمــات الصحيــة يف تربيــز منخفضــة، وأن صانعــي السياســات بحاجــة إىل توظيــف سياســات مناســبة لتحســن معانــاة املــرىض مــن اخلدمــات الصحيــة.

ABSTRACT This study investigated public trust in health services in Tabriz, Islamic Republic of Iran. A cross- sectional household study was conducted in 2014, using random cluster sampling. A total of 1050 households were enrolled in the study and a valid questionnaire was used to collect data through interviews. The mean score for public trust in health services in Tabriz (out of 100) was 53.91 ± 13.7. People had most trust in professional expertise and lowest in macro-level policy. Specialists, pharmacy doctors and nurses were the health providers that enjoyed the highest levels of trust. It is concluded that public trust in health services in Tabriz is low and policy-makers need to employ appropriate policies to improve patients’ experience of health services.

Confiance du public iranien dans les services de santé : données recueillies à Tabriz (République islamique d'Iran)

RÉSUMÉ La présente étude visait à étudier la confiance du public dans les services de santé de Tabriz, en République islamique d’Iran. Une étude transversale des ménages a été conduite en 2014, à l’aide d’un sondage aléatoire par grappe. Un total de 1050 ménages ont participé à l’étude, et un questionnaire validé a été utilisé pour collecter des données au cours d’entretiens. Le score moyen de la confiance du public dans les services de santé à Tabriz (sur un échantillon de 100 individus) était de 53,91 ± 13,7. Les individus faisaient davantage confiance à l’expertise professionnelle et se fiaient moins aux politiques concernant les soins de santé dans leur ensemble. Les spécialistes, les docteurs en pharmacie et les personnels infirmiers étaient les prestataires de santé qui jouissaient des taux de confiance les plus élevés. En conclusion, on peut dire que la confiance du public dans les services de santé à Tabriz est basse et que les responsables politiques doivent recourir à des politiques appropriées pour améliorer l’expérience des services de santé vécue par les patients.

1Tabriz Health Service Management Research Centre, Department of Health Service Management, School of Health Management and Medical Informatics, Tabriz University of Medical Sciences, Tabriz, Islamic Republic of Iran. 2Iranian Center of Excellence in Health Management, Department of Health Service Management, School of Health Management and Medical Informatics, Tabriz University of Medical Sciences, Tabriz, Islamic Republic of Iran (Correspondence to: M. Saadati: [email protected]). 3Road Traffic Injury Research Center, Department of Statistics and Epidemiology, Faculty of Health, Tabriz University of Medical Sciences, Tabriz, Islamic Republic of Iran. 4Department of Statistics and Epidemiology, Faculty of Health, Tabriz University of Medical Sciences, Tabriz, Islamic Republic of Iran. 5Department of Health Service Management, School of Health Management and Medical Informatics, Tabriz University of Medical Sciences, Tabriz, Islamic Republic of Iran. Received: 24/05/15; accepted: 03/07/16

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Introduction Previous studies have identified six and NGO providers are active in the dimensions of public trust in health various levels of health care in Tabriz. Trust is a major factor in all human care: patient centredness, macro-level interactions (1), and has long been policies, professional expertise of health recognized as a cornerstone of effec- care providers, quality of care, informa- Materials and methods tive relationships between patients tion provision and communication, and and health care providers (2). In the quality of cooperation between health A cross-sectional household study context of health care, there are two care providers (6,7). Studies of public was conducted in summer 2014, us- forms of trust: interpersonal and pub- trust in the Australian health system ing random cluster sampling. The list lic. Interpersonal trust is trust placed found a moderate level of trust, which of addresses and telephone numbers by one person in another and can be varied slightly from 3.3 to 3.6 out of for Tabriz households in 2013 was 5 over the years (10). A comparative described as “the optimistic acceptance used as the sampling framework, study of public trust in health care in of a vulnerable situation in which the and 1050 households (70 clusters of Germany, the Netherlands, and Eng- truster believes the trustee will care for 15 households) were included in the the truster’s interests” (3, 4). Public trust land and Wales showed that the Dutch study. Clusters were selected based on is trust placed by a group or a person in had the most trust in the “patient focus probability proportional to size (PPS). a societal institution or system, such as of providers” and the Germans the The starting-point (household) within the health system, Public trust in health least. In all the countries, public trust in care has been defined as confidence macro-level policies was low. German each cluster was determined using the that those in need of health care will respondents had significantly less trust sampling framework, and then the next be sufficiently cared for and treated (5, in “health care providers’ professional nearest household to the right of the 6). It is a general attitude influenced by expertise” and “quality of care”. The starting-point was included, until a total people’s experiences with the health Dutch people had significantly more of 15 was reached. Households that care system (7). trust in “information supply and com- had been established in Tabriz for at Public trust can be influenced by the munication” and “quality of coopera- least six months and that were willing health care system in two ways: through tion”. Moreover, people in England and to participate in the study were con- institutional guarantees (regulation Wales placed significantly more trust in sidered as eligible. The study objectives of health care providers, protection of family physicians, specialists, dentists were explained to the respondents, then patients’ rights, etc.) and through the and non-medical complementary or face-to-face interviews were carried out availability of high quality health care (8, alternative therapists than the Dutch with the head of household, or another 9). Cultural factors and the organization and German respondents (7). member of the household, by a trained of the health care system may also affect A low level of therapeutic success questioner. public trust (7). and compliance with treatment advice The questionnaire had two sections: The health system in the Islamic could lead to low levels of trust (8). the first dealt with the demographics Republic of Iran, as in other countries, Generally, a negative experience in a pa- and socioeconomic situation of the tries to achieve public satisfaction and tient–provider contact may lead to low households (6 questions) (15) and the trust. The Ministry of Health and Medi- satisfaction and trust. Measurement of second was a two-part questionnaire cal Education is responsible for this public trust in health care provides the about public trust, developed by Van issue. In each province there is a medi- government with information on the der Schee et al. (7). The questionnaire cal university, which is responsible for performance of the health system from was translated into Persian using the the users’ perspective ( ) on two lev- public health, service provision in public 12 double forward-backward method. It els. First, on the macro-level, public trust facilities, supervision of health provid- was validated for reliability through a is a supporting indicator for changes in ers (including those in the private sec- pilot study of 30 households (Cron- the health system. Secondly, on the mi- tor, charities and Non-Governmental bach's alpha = 0.86) and for validity cro-level, the level of user trust in health Organization (NGOs)) and medical through a Delphi study of expert opin- education. Primary health care services care is likely to affect their attitudes and ion (content validity ratio (CVR) = are provided through a nationwide behaviour in practice (6,13,14). 0.81). The six dimensions of the ques- network of facilities. Almost 90% of The aim of this study was to deter- tionnaire were: people have insurance coverage (10). mine public trust in health services in The health achievements of the Iranian Tabriz, the capital city of East Azerbai- • patient centredness (five questions, health system have been encouraged by jan province of the Islamic Republic of including items such as taking pa- WHO (11). Iran. Governmental, private, charitable tients seriously, attention);

714 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

• macro-level policies concerning Results in relation to the job of the head of the health care (three questions on cost household. policies, waiting times and quality); Most of the respondents (73.8%) were Having insurance or a history of • professional expertise of health pro- female and 84.2% had no university edu- hospitalization had no significant ef- viders (three questions on knowl- cation. The mean age of the respondents fect on trust level (P > 0.05). One-way edge, training and education of was 38.6 years (range 15–88 years). ANOVA showed that only in the di- doctors, and use of new treatments); Only 19.8% of households were renters mensions of professional expertise (P = and 81.1% had social insurance. About 0.048) and cooperation between health • quality of care (six questions on pre- half (48.5% and 52%, respectively) of care providers (P = 0.002) there was a scribing of the right dose at the right significant difference between groups time for patients, testing, etc.); the households evaluated their eco- nomic condition and job classification with different job values. As shown in • information provision and commu- as average for the community. House- Table 3, the people of Tabriz were most nication (five questions on whether holds’ mean self-reported economic trusting of specialists, pharmacy doctors patients are provided with clear in- capacity (out of 100) was 57.55 ± 18.43. and nurses. formation about various treatments, patient education); and The mean level of public trust in health services in Tabriz was 53.91±13.7 (out • quality of cooperation between health of 100). Table 1 shows the mean level of Discussion care providers (three questions). public trust for the six dimensions. A four-point Likert scale was used to The study revealed a low level of public rank respondents’ trust from very low to One-way ANOVA showed a signifi- trust. The people of Tabriz had the high- very high. Respondents were asked to cant difference in public trust on all the est mean level of trust in professional rank their trust based on their general dimensions between different econom- expertise and the lowest in macro-level experience with health services (public ic groups (P < 0.001); households with policies. Meyer (16) reported that peo- and private). They also had the option a lower economic capacity had more ple were distrustful of the government of selecting "no opinion". trust in health services. A significant role in the health system, and suggested Respondents were also given a list of difference was also observed between that a low level of public trust might be 14 health providers and institutions and age groups, with older people having a a result of the increasing cost of health asked to grade their trust in them from 1 higher level of trust (Table 2). services and the weak and inequitable (very low) to 20 (very high). There was also a significant dif- performance of health insurance. The Data analysis was done using SPSS ference in trust (P < 0.001) accord- existence of informal payments and 21. Descriptive statistics, as well as the ing to education level of the head of disregard for patients’ right could be independent t-test and one-way analysis household, both in total trust and for other reasons. Public trust in health of variance (ANOVA), were used, as each of the dimensions except profes- services is measured regularly in various appropriate. The study was approved sional expertise (P = 0.191). Individu- countries (17). It is used as an indicator by the ethical committee of Tabriz Uni- als with a doctorate, and those who of public support and an important fac- versity of Medical Sciences. This paper were illiterate or had only elementary tor in policy-making and governance, was a part of larger study, the Tabriz education, had the most trust in health to orient the future performance of the Clinical Governance Research Project services (74.2±11.8, 56.11±15.21 and health care system (6,7). A comparative (TCGRP), which has been described 55.42±13.15, respectively). No signifi- study of three countries showed that elsewhere (15). cant difference in public trust was seen the inhabitants of England and Wales

Table 1. Mean level of public trust in the six dimensions of health care services, Tabriz Dimension Mean trust a Standard deviation Patient focus of health providers 52.46 23.32 Macro-level policies 34.71 19.08 Professional expertise 61.76 20.70 Quality of care 59.36 16.57 Information provision and communication 53.40 21.59 Quality of cooperation between health care providers 58.13 17.69

a Out of 100.

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Table 2. Public trust in health services according to household’s economic capacity and age group of respondent Household economic capacity Mean trust a Standard deviation P value b Very low 65.73 11.40 Low 55.07 13.51 Average 55.65 12.99 < 0.001 Good 52.14 15.12 Excellent 47.49 14.39 Age of respondent (years) <20 52.86 14.77 21–40 51.44 13.80 < 0.001 41–60 54.33 13.84 61–80 59.57 13.10

a Out of 100. b Based on one-way ANOVA.

had most trust in the health care sys- regard, a low level of public trust could the highest level of trust. This might be tem, followed by the Dutch. People in be a result of low patient satisfaction related to sample size, since the number Germany generally had the least trust in and poor performance of health care of individuals with this level of educa- health care (7). The Dutch respondents organizations (19). Moreover, as a tion was very low. rated their trust in the health services as study of 33 countries concluded (20), The people of Tabriz had most trust 7 out of 10, which is higher than the level a low level of trust may stem from the in specialists, pharmacy doctors, nurses found in our study. The study by Van incapacity of the health system to em- and general physicians. This is similar der Schee et al. revealed a mean level of ploy proper policies to improve public to the findings in England and Wales, public trust of 5.05 in the Netherlands health. This study, and the Dutch study Germany and the Netherlands, where (18). It was suggested that the level of showed that older people have signifi- it was also found that therapists who trust is related to patients’ compliance cantly more trust in health services that were not doctors had the lowest trust of with medical advice and therapeutic younger people (20). Furthermore, in all health care providers (7). Tabriz is a success (8). the Netherlands, individuals with lower medical tourism destination for people In the health sector, trust has long education had a higher level of trust from the north-west of the Islamic Re- been recognized as crucial in the pa- (6). Our results were similar, although public of Iran, Azerbaijan and Turkey. tient–provider relationship. In this people with a postgraduate degree had It is possible that the high occurrence of

Table 3. Level of public trust in specific health care providers Health care provider Mean trusta Standard deviation Public hospital 12.20 5.55 Private hospital 12.59 6.39 Social security hospital 11.23 7. 0 Urban health centre 10.83 7.01 Private clinic 12.87 5.99 Medical university clinic 7.68 7.59 General physician 13.11 5.34 Specialist 14.94 5.39 Nurse 13.28 6.09 Dentist 12.70 6.37 Pharmacy doctor 14.20 5.30 Physiotherapist 9.62 7.99 Herbal apothecary 10.80 7.51 Traditional provider (e.g. bonesetter) 9.08 7.70

a Out of 20.

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medical tourism involving the special- and have opportunities to influence have further implications for trust in ists in Tabriz has created more trust care decisions. This results in a patient- the health system and in government. A in them. In addition, the poor perfor- centred approach and more trust in high level of public trust is desirable be- mance of the referral system means that health care providers (24,25). Provision cause of the universal value of health. It many patients go directly to specialists. of information and communication in It is also common in Tabriz for patients health services was ranked fifth of the six is suggested that a national study should to go directly to a pharmacy, where they dimensions of public trust. This suggests be conducted on public trust and its can explain their problem and receive that people in Tabriz have poor expe- determinants, to identify the challenges the drugs they need. This might be a riences of communication in health and develop appropriate strategies. A fo- service facilities. Since trust is a result of result of the high cost of a visit to a doc- cus on professional ethics, observation patient satisfaction and may affect other tor, long waiting times or absence of of patients’ rights and the establishment insurance coverage, and could be the aspects of the health services, decision- of an electronic health records system reason why a high level of trust is placed makers need to consider the factors in pharmacy doctors. that affect trust and establish plans to in order to improve cooperation among increase public trust in health care. A qualitative study in South Aus- physicians could be useful. tralia concluded that patients had the Limitations of the study same level of trust in public and private To the best of our knowledge, this study Acknowledgements hospitals (21). Similarly, our study re- is one of the first on public trust in health vealed the same trust in private and pub- care in the Islamic Republic of Iran. It The authors thank the Tabriz house- lic hospitals. These results are in contrast relied on self-reported information of holds that participated in the study. with those of Hardie & Crichley, which households, which might be biased. showed different levels of trust between Funding: This study was funded by the public and private hospitals (22). Tabriz Health Services Management Trust is the cornerstone of an ef- Conclusion and Research Centre, Tabriz University of fective patient–physician relationship recommendation Medical Science, Tabriz, Islamic Re- (2,23). In communication between pa- tients and physicians, patients must be The level of public trust in health ser- public of Iran. given important medical information vices was low in Tabriz. This might Competing interests: None declared.

References

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17. European Opinion Research Group EEIG. Standard Eurbarom- for trust considerations in South Australia. BMC Health Serv eter 60. Public opinion in the European Union. Brussels: Euro- Res. 2015 Jul 30;15(1):297. PMID:26223973 pean Commission; 2003 (http: ec.europa.eu/public_opinion/ 22. Hardie EA, Critchley CR. Public perceptions of Australia’s doc- archives/eb/eb60/eb60_rapport_standard_en.pdf) tors, hospitals and health care systems. Med J Aust. 2008 Aug 18. van der Schee E, Groenewegen PP. Determinants of public 18;189(4):210–4. PMID:18707565 trust in complementary and alternative medicine. BMC Public 23. Yuan W, Guan D, Lee S, Lee Y-K. The role of trust in ubiquitous Health. 2010 Mar 12;10:128. PMID:20226015 healthcare. Seoul: Ministry of Information and Communica- 19. Goold SD. Trust and the ethics of health care institutions. Hast- tion; 2007. ings Cent Rep. 2001 Nov-Dec;31(6):26–33. PMID:12945452 24. Sofaer S, Firminger K. Patient perceptions of the quality of 20. Elgar FJ. Income inequality, trust, and population health in health services. Annu Rev Public Health. 2005;26:513–59. 33 countries. Am J Public Health. 2010 Nov;100(11):2311–5. PMID:15760300 PMID:20864707 25. Tabrizi JS, Sadeghi-Bazargani H, Saadati M. Development of 21. Ward PR, Rokkas P, Cenko C, Pulvirenti M, Dean N, Carney S, et performance indicators for patient and public involvement in al. A qualitative study of patient (dis)trust in public and private hospital: expert consensus recommendations based on the hospitals: the importance of choice and pragmatic acceptance available evidence. J Clin Res Gov. 2013;2(1):26–30.

718 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Tobacco chewing and risk of gastric cancer: a case– control study in Yemen F.A. Al-qadasi 1, S.A. Shah 1,2, H.F. Ghazi 3

مضغ التبغ وخطر اإلصابة برسطان املعدة: دراسة حاالت وشواهد يف اليمن فاروق القديس، شمسول شاه، حسنني غازي هدفــتاخلالصــة: هــذه الدراســة إىل تقييــم عوامــل خطــر اإلصابــة برسطــان املعــدة يف اليمــن. حيــث أجريــت دراســة حــاالت وشــواهد يف املستشــفيات لـــ 70 حالــة و 140 ً شــاهدايف مدينــة صنعــاء مــا بــني مايو/أيــار وأكتوبر/ترشيــن األول مــن عــام 2014. وقــد اســتخدم اســتبيان َّمنظــم جلمــع املعلومــات مــن خــال مقابلــة مبــارشة. فكانــت العوامــل اهلامــة خلطــر اإلصابــة برسطــان املعــدة َالعيــش يف املناطــق الريفيــة، ومضــغ التبــغ، ورشب امليــاه غــر املعاجلــة. وكانــت كثــرة اســتهلك الدجــاج واجلبــن واحلليــب واخلضــار النشــوية واخليــار واجلــزر والكــراث والفلفــل احللــو ومرشوبــات الفواكــه والبقوليــات وزيــت الزيتــون مرتافقــة مــع انخفــاض ملحــوظ يف خطــر اإلصابــة برسطــان املعــدة. وأظهــر حتليــل ّالتحــوف اللوجســتي املتعــدد أن مضــغ التبــغ وكثــرة اســتهلك اخلبــز األبيــض كانــا مرتبطــني مــع زيــادة خطــر اإلصابــة برسطــان املعــدة، يف حــني كانــت هنــاك علقــة عكســية مــع كثــرة اســتهلك الدجــاج والبطاطــا املطبوخــة ومرشوبــات الفواكــه. يمكــن الوقايــة مــن خطــر اإلصابــة برسطــان املعــدة عــن طريــق التثقيــف الصحــي وزيــادة الوعــي املجتمعــي.

ABSTRACT This study aimed to assess the risk factors for gastric cancer in Yemen. A hospital-based case–control study of 70 cases and 140 controls was carried out in Sana’a city between May and October 2014. A structured questionnaire was used to collect information through direct interview. Living in rural areas, tobacco chewing and drinking untreated water were significant risk factors for gastric cancer. Frequent consumption of chicken, cheese, milk, starchy vegetables, cucumber, carrots, leeks, sweet pepper, fruit drinks, legumes and olive oil were associated significantly with decreased risk of gastric cancer. Multiple logistic regression analysis showed that chewing tobacco and frequent consumption of white bread were associated with increased risk of gastric cancer, whereas frequent consumption of chicken, cooked potatoes and fruit drinks had an inverse association. Risk of gastric cancer can be prevented by health education and increasing community awareness.

Tabac à chiquer et risque de cancer de l’estomac : étude cas-témoin au Yémen

RÉSUMÉ La présente étude avait pour objectif d’évaluer les facteurs de risque du cancer de l’estomac au Yémen. Une étude cas-témoin en milieu hospitalier impliquant 70 cas et 140 témoins a été menée dans la ville de Sanaa entre mai et octobre 2014. Un questionnaire structuré a été utilisé pour collecter des informations au cours d’entretiens directs. La résidence en zone rurale, la consommation de tabac à chiquer et d’eau de boisson non traitée constituaient des facteurs de risque significatifs pour le cancer de l’estomac. Une consommation fréquente de poulet, de fromage, de lait, de légumes riches en amidon, de concombres, de carottes, de poireaux, de poivrons, de boissons fruitées, de légumes et d’huile d’olive était fortement associée à une diminution du risque de cancer de l’estomac. L’analyse de régression logistique multiple a montré que le tabac à chiquer et une consommation fréquente de pain blanc étaient associés à une augmentation du risque de cancer de l’estomac, tandis que la consommation fréquente de poulet, de pommes de terre cuites et de boissons fruitées avait une association inverse. Il est possible de prévenir le risque de cancer de l’estomac grâce à une éducation en santé et à la sensibilisation de la communauté.

1Department of Community Health, Faculty of Medicine, University of Science and Technology, Sana'a, Yemen (Correspondence to: S.A. Shah: [email protected] ); 2Medical Molecular Biological Institute, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia. 3Community Medicine Unit, International Medical School, Management and Science University, Shah Alam, Selangor, Malaysia. Received: 22/09/15; accepted: 31/08/16

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Introduction number of cancer cases), making it the Methods seventh most common malignancy in Gastric cancer is a major contributor both sexes. In men, it was the sixth most Study design and sampling to mortality and morbidity worldwide. common malignancy with 279 new This study was a hospital-based case– GLOBOCAN 2012 reported 952 000 cases per 100 000 (5.2% of the total) but control study that was carried out in new cases of gastric cancer in 2012 in women, it was the 11th most com- Sana’a City. The cases were all patients (6.8% of the total number of cancer mon malignancy with 143 new cases who had histologically confirmed gas- cases), making it the fourth most com- per 100 000 (2.4% of the total) (1). A tric cancer, collected from the National mon malignancy in men and the fifth Oncology Centre in Sana’a City, which most common in women worldwide. study done in Hadramout, Yemen, in is a specialized centre that receives refer- More than 70% of cases occurred in 2006, showed that gastric cancer was rals from hospitals for chemotherapy developing countries, and about half of the second most common type of gas- and radiotherapy. The controls were the global total occurred in East Asia trointestinal cancer after colorectal can- (mainly in China). Gastric cancer was cer. It was the sixth most common type collected from the two major hospitals the third leading cause of cancer death of all cancers among men and the ninth in Sana’a City (Al-Thawra and Al- Jomhori) from where the cases were in both sexes worldwide in 2012 (723 among women (8). In Yemeni society, referred. The controls were selected ran- 000 deaths, 8.8% of the total) (1). Gas- the habit of chewing khat (Catha edulis) domly from outpatient clinics (5.3%) tric cancer shows regional variations is highly prevalent among adults of both or inpatient departments (medical because of differences in dietary pat- sexes and most of them start chewing terns, and the prevalence of Helicobacter 57.6%, surgical 31.1% and gynaecologi- in childhood. It is estimated that up to pylori infection (2). There has been a cal 6.1%) during the study period. The steady decline in recent years in most 90% of adult men, 73% of women, and controls were free from any malignant developed countries and in countries 15–20% of children under the age of 12 tumours or digestive tract disorders, with high incidence rates in Asia (Ja- years in Yemen chew khat (9). There and matched to cases for age (± 5 years) pan, China and Korea), Latin America are three main alkaloids present in khat and gender. The case to control ratio (Colombia and Ecuador) and Europe leaves: cathinone, norpseudoephedrine was 1: 2. Patients with other concurrent (Ukraine) (3). (cathine), and norephedrine (10). Khat types of cancer were excluded. Gastric cancer is a multifactorial dis- is exposed to carcinogenic substances, ease. A positive family history of gastric such as fertilizers, herbicides and pes- Data collection cancer has been associated with a two- ticides, that are widely used by farmers The data were collected between May to threefold increased risk of the disease, in Yemen to ensure that they have > and October 2014. A structured ques- which suggests a genetic basis (4). Diet 1 harvest a year (11). Khat chewing is tionnaire was used to collect informa- is considered to play an important role concurrently used with tobacco smok- tion through direct interview about in the occurrence of gastric cancer. Salty ing, which may increase the burden of the risk factors for gastric cancer from food and smoked or marinated food cases and controls. The questionnaire deficient in vitamins and antioxidants cancer. included: general characteristics (age, significantly increases the probability of No studies have focused on risk fac- sex, marital status, occupation, income, gastric cancer (4-6). Vegetables, espe- tors of gastric cancer in Yemen. The house ownership, residence and edu- cially nonstarchy and allium vegetables, Yemeni people have particular habits cational level); special habits (smoking fruits and pulses (legumes) decrease the such as chewing khat and tobacco, risk of gastric cancer (5), and green tea and khat and tobacco chewing); past which is also called shamma (a type of history of peptic ulcer or comorbidity; also reduces the risk. Antioxidants such tobacco that is put between the lip and as vitamins C and E, β-carotene, or mi- family history of gastric cancer or other tongue or above the tongue). Therefore, cronutrients such as zinc or magnesium malignant tumours; source of drinking it is pertinent that we explore the asso- have been shown to have protective water; and history of consumption of 41 effects against gastric cancer 7( ). ciation of khat and tobacco with gastric different types of grains, fruits and veg- cancer. This study was conducted to The National Cancer Registry in etables. Dietary history was collected Yemen is not comprehensive and there assess the risk factors for gastric cancer by validated questionnaire taken from are no reliable data available. According in Yemen, especially to identify the as- Cancer Council, Australia (12) and to GLOBOCAN 2012, the incidence sociation between gastric cancer and modified for the diet in Yemen. Cron- of gastric cancer in Yemen was 422 new khat and tobacco chewing and certain bach’s α for the modified questionnaire cases per 100 000 (3.7% of the total dietary factors. was 0.79.

720 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Operational definition of Data analysis Ethical consideration variables SPSS version 21 was used to analyse The study was reviewed and approved The dependent variable was gastric the data. Frequency (%) was used to by the Medical Research Ethics Commit- tee, Department of Scientific Research, cancer that was confirmed histo- describe the qualitative variables, and University of Science and Technol- logically by biopsy at any stage. The mean and standard deviation (SD) independent variables were sociode- ogy, Sana’a City, Yemen (approval No were used to describe the quantitative mographic factors such as education 03/2014). status, occupation, house ownership, variables. Odds ratios (OR) and 95% confidence intervals (CIs) were calcu- history of smoking, tobacco and khat Results chewing, family history of gastric cancer lated to measure the risk. The 2χ and or other cancers, and source of drinking Fisher’s exact tests were used to show The demographic features of the cases water (treated and untreated water). the significance of association between and controls are shown in Table 1. There Diet was categorized into three classes cases and controls and the risk factors were 70 cases and 140 controls, with according to consumption frequency for gastric cancer at a significance level a mean (SD) age of 57.9 (12.79) and (never, infrequent; once monthly, 2 or of 0.05. Multiple logistic regression was 57.6 (11.80) years, respectively. Men 3 times per month, 1–6 times per year, constituted 67.1% of the gastric cancer used to calculate adjusted odds ratio 7–11 times per year; and frequent; once patients and 72.1% of the controls. Cas- daily, ≥ 2 times daily, 1 or 2 times per and the corresponding 95% CI for gas- es were slightly less educated compared week, 3 or 4 times per week, 5 or 6 times tric cancer in relation to exposures of with the controls, but there were no sig- per week). interest. nificant associations between cases and

Table 1 Sociodemographic characteristics of study participants Variable Cases Controls P value OR 95% CI (n = 70) (n = 140) Mean (SD) Freq % Mean (SD) Freq % Lower Upper Age (yr) 57.9 (12.79) 57.6 (11.80) < 45 8 11.4% 14 10.0% 0.729 Ref 45–64 38 54.3% 84 60.0% 0.79 0.31 2.05 ≥ 65 24 34.3% 42 30.0% 1.00 0.37 2.73 Sex 0.521 0.79 0.42 1.47 Male 47 67.1% 101 72.1% Female 23 32.9% 39 27.9% Education status 0.880 1.07 0.44 2.62 Lower education 62 88.6% 123 87.9% Higher education 8 11.4% 17 12.1% Marital status 0.755 1.16 0.45 2.97 Married 63 90.0% 124 88.6% Unmarried 7 10.0% 16 11.4% Occupation 0. 314 Unemployed 1 1.4% 9 6.4% Ref Non-professional 66 94.3% 126 90.0% 4.71 0.59 38.01 Professional 3 4.3% 5 3.6% 5.40 0.44 66.67 Residence 0.036 1.91 1.04 3.51 Rural 49 70.0% 77 55.0% Urban 21 30.0% 63 45.0% House ownership 0.120 1.94 0.83 4.51 Yes 62 88.6% 112 80.0% No 8 11.4% 28 20.0%

CI = confidence interval; Freq = frequency; OR = odds ratio; Ref = reference; SD = standard deviation.

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controls regarding educational status, consumption of white bread were as- family history of cancer and gastric can- marital status, occupation and house sociated significantly with the odds of cer, which is similar to our study (13, ownership. Those who lived in rural having gastric cancer. 21). Other studies have shown that peo- area had 2 times greater odds of having Our study showed that people who ple with a positive family history of gas- gastric cancer. lived in rural areas had greater odds of tric cancer had greater odds of having There were no significant associa- having gastric cancer. This was contrary cancer, thus reflecting the importance tions between tobacco smoking, dura- to other studies that reported no signifi- of hereditary and environmental factors tion of smoking, and number of cigarette cant association between residence and in the occurrence of gastric cancer (4, packs per day and the occurrence of gastric cancer (13, 14). The possible ex- 22-25). gastric cancer. The odds of gastric can- planation for this may be that in a coun- Drinking untreated water was a cer were 3 times higher among those try such as Yemen, access to healthcare significant risk factor for gastric can- who chewed tobacco than non-chewers facilities is limited in rural areas. cer, which could have been because of but there was no significant association Chewing tobacco (shamma) was higher levels of nitrates in untreated with the duration of chewing tobacco. an important risk factor for gastric can- water (18). There were nonsignificant associations cer in the present study. This could have Our study revealed that frequent between cases and controls regarding been because the contents of shamma consumption of vegetables such as chewing khat, years and hours of chew- were swallowed during chewing, thus starchy vegetables, cucumber, carrots, ing khat, past history of peptic ulcer, entering the stomach. In a previous leeks, sweet pepper, and fruit drinks ap- and family history of gastric or other study in Yemen, H. pylori infection was peared to be protective factors against cancer. The main source of drinking wa- strongly associated with the habit of gastric cancer. Fruits and vegetables ter was untreated in 87.1% of the cases chewing tobacco and H. pylori infection are rich sources of dietary fibre, miner- and in 70.0% of the controls and those is an important risk factor for gastric als, and antioxidants such as ascorbic who drank untreated water had 3 times cancer (15). Although we reported that acid, which may inhibit initiation or greater odds of gastric cancer (Table 2). tobacco smoking had no significant progression of cancer (25). The major- Regarding dietary habits, the fol- relationship with gastric cancer, which ity of epidemiological studies in gastric was similar to another study ( ), most lowing foods had a significant inverse 16 cancer have reported similar results (13, other studies revealed a significantly association with gastric cancer: chicken, 16, 18, 19, 21, 22, 24, 26, 27). However, increased risk of gastric cancer with dairy products such as cheese and milk, in another study, potatoes were a signifi- smoking (13, 17). The risk increases vegetables such as sauced or cooked cant risk factor (13). In a large cohort significantly with the quantity and du- potatoes, cucumber, carrots, leeks, in the United States of America, no as- ration of smoking (18, 19). Regard- sweet pepper, fruit drinks, legumes such sociations were found between fruit and ing khat chewing, our study showed a as beans, peas and lentils, and olive oil vegetable intake and gastric cancer risk nonsignificant association with gastric (Table 3). (28). Although previous studies have cancer. This could have been because In multiple logistic regression analy- reported the protective role of allium of the high prevalence of khat chewing sis, people who chewed tobacco had vegetables (garlic and onion) in gastric 4.4 times greater odds of having gas- among the cases and controls. Although no previous studies have explored the cancer (5, 24, 26), we did not find such tric cancer. Frequent consumption of a relationship. chicken, sauced or cooked potatoes and association between gastric cancer and Our study showed that frequent fruit drinks was significantly associated khat chewing, some have shed light on consumption of legumes such as beans, with a decrease in the OR (95% CI) this association. One such study report- peas and lentils had a protective effect of gastric cancer: [0.08 (0.03–0.22), ed that the high tannin content of khat against gastric cancer. These soya prod- 0.19 (0.05–0.68) and 0.26 (0.09–0.76), leaves thickens the oesophageal and ucts contain considerable amounts of respectively]. Frequent consumption of gastric mucosa, which possibly causes saponins and isoflavones, which have white bread was significantly associated oesophageal and gastric carcinoma. The been shown to possess anticarcinogenic with a twofold increase in the odds of authors found an increase in cancer effects 5( ). These results are similar to gastric cancer (Table 4). of the cardia and gastro-oesophageal junction in individuals who chewed many previous studies (13, 21, 24). khat and smoked water pipes, but the We found that consumption of Discussion sample size was insufficient to identify white bread was significantly associated the effects of the two factors 20( ). with increased odds of gastric cancer. Living in a rural area, chewing tobacco, Some studies have revealed a Bread is one of the essential sources of drinking untreated water, and frequent nonsignificant association between salt worldwide and its salt content can

722 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Table 2 Special habits, family history of gastric or other cancers, and source of drinking water Variable Cases Controls P value OR 95% CI (n = 70) (n = 140) Freq % Freq % Lower Upper Smoking 0.063 1.74 0.97 3.11 Yes 43 61.4% 67 47.9% No 27 38.6% 73 52.1% Duration of smoking (yr) 0.650 1.20 0.55 2.59 > 20 25 58.1% 36 53.7% ≤ 20 18 41.9% 31 46.3% No. of cigarettes (packs/day) 0.523 1.42 0.49 4.14 ≥ 1 7 24.1% 11 18.3% < 1 22 75.9% 49 81.7% Tobacco chewing (shamma) < 0.001 3.35 1.71 6.55 Yes 26 37.1% 21 15.0% No 44 62.9% 119 85.0% Years of tobacco chewing 0.626 1.33 0.42 4.24 > 20 13 50.0% 9 42.9% ≤ 20 13 50.0% 12 57.1% Khat chewing history 0.069 1.85 0.95 3.62 Yes 55 78.6% 93 66.4% No 15 21.4% 47 33.6% Years of khat chewing 0.478 0.69 0.31 1.49 > 20 41 74.5% 74 79.6% ≤ 20 14 25.5% 19 20.4% Duration of chewing khat h/session 0.493 1–3 20 36.4% 28 30.1% Ref 4–6 29 52.7% 58 62.4% 0.70 0.34 1.45 > 6 6 10.9% 7 7.5% 1.20 0.35 4.11 Frequency of chewing Frequent 54 77.1% 92 65.7% 0.090 1.76 0.91 3.40 Never or infrequent 16 22.9% 48 34.3% Past history of peptic ulcer 0.363 1.31 0.73 2.37 Yes 29 41.4% 49 35.0% No 41 58.6% 91 65.0% Family history of gastric cancer 0.071 4.28 1.04 17.66 Yes 6 8.6% 3 2.1% No 64 91.4% 137 97.9% Degree of relative 0.333 NA 1st 6 100.0% 2 66.7% 2nd 0 0.0% 1 33.3% Family history of other cancer 0.688 1.17 0.54 2.55 Yes 12 17.1% 21 15.0% No 58 82.9% 119 85.0% Source of drinking water 0.006 2.90 1.32 6.39 Untreated 61 87.1% 98 70.0% Treated 9 12.9% 42 30.0%

CI = confidence interval; Freq = frequency; NA = not applicable; OR = odds ratio; Ref = reference.

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Table 3 Food risk factors for gastric cancer Food Cases Controls P value OR 95% CI Freqa % Freq % Lower Upper Corn 43 61.4% 82 58.6% 0.691 1.13 0.63 2.03 Barley 15 21.4% 28 20.0% 0.809 1.09 0.54 2.21 Stored grains 19 27.1% 36 25.7% 0.824 1.08 0.56 2.06 Cooked red meat 31 44.3% 69 49.3% 0.494 0.82 0.46 1.46 Chicken 7 10.0% 61 43.6% < 0.001 0.14 0.06 0.34 Sauced fish 10 14.3% 21 15.0% 0.891 0.94 0.42 2.13 Grilled fish 11 15.7% 16 11.4% 0.384 1.44 0.63 3.31 Cheese 21 30.0% 79 56.4% < 0.001 0.33 0.18 0.61 Milk 46 65.7% 110 78.6% 0.046 0.52 0.28 0.99 Yogurt 62 88.6% 126 90.0% 0.750 0.86 0.34 2.16 Sauced or cooked potatoes 58 82.9% 134 95.7% 0.003 0.22 0.08 0.60 Fried potatoes 17 24.3% 51 36.4% 0.078 0.56 0.29 1.07 White bread 44 62.9% 68 48.6% 0.052 1.79 1.00 3.22 Macaroni 23 32.9% 57 40.7% 0.270 0.71 0.39 1.30 Mandarin 11 15.7% 24 17.1% 0.793 0.90 0.41 1.96 Orange 15 21.4% 48 34.3% 0.057 0.52 0.27 1.02 Lemon 31 44.3% 55 39.3% 0.488 1.23 0.69 2.20 Banana 41 58.6% 70 50.0% 0.242 1.41 0.79 2.52 Apple 16 22.9% 46 32.9% 0.136 0.61 0.31 1.17 Pomegranate 12 17.1% 23 16.4% 0.896 1.05 0.49 2.26 Guava 7 10.0% 24 17.1% 0.174 0.54 0.22 1.32 Grape 21 30.0% 49 35.0% 0.469 0.80 0.43 1.48 Fruit drink 8 11.4% 34 24.3% 0.032 0.40 0.18 0.92 Garlic 41 58.6% 90 64.3% 0.421 0.79 0.44 1.41 Onion 42 60.0% 95 67.9% 0.261 0.71 0.39 1.29 Cucumber 46 65.7% 111 79.3% 0.034 0.50 0.26 0.95 Carrots 44 62.9% 117 83.6% 0.001 0.33 0.17 0.64 Leek 48 68.6% 121 86.4% 0.003 0.34 0.17 0.69 Sweet pepper 43 61.4% 105 75.0% 0.044 0.53 0.29 0.98 Chilli pepper 57 81.4% 110 78.6% 0.629 1.20 0.58 2.47 Beans/ pea/lentil 58 82.9% 130 92.9% 0.030 0.37 0.15 0.91 Almond 2 2.9% 12 8.6% 0.136 0.31 0.07 1.44 Honey 9 12.9% 31 22.1% 0.110 0.52 0.23 1.16 Eggs 51 72.9% 117 83.6% 0.070 0.53 0.26 1.05 Olive oil 14 20.0% 49 35.0% 0.027 0.46 0.24 0.92 Animal ghee 48 68.6% 81 57.9% 0.134 1.59 0.87 2.91 Sweets 46 65.7% 106 75.7% 0.128 0.61 0.33 1.15 Salta 56 80.0% 98 70.0% 0.125 1.71 0.86 3.41 Fahsa 8 11.4% 31 22.1% 0.064 0.45 0.20 1.05 Tea 63 90.0% 132 94.3% 0.261 0.55 0.19 1.57 Coffee 59 84.3% 129 92.1% 0.085 0.46 0.19 1.12

aHow many times each food item was taken. CI = confidence interval; OR = odds ratio.

724 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Table 4 Multivariate analysis of risk factors for gastric cancer Variables B SE P value AOR 95% CI Lower Upper Tobacco chewing (Shamma) 1.53 0.42 < 0.001 4.37 1.92 9.95 Family history of gastric cancer 1.68 0.85 0.064 4.81 0.91 25.28 Chicken −2.52 0.50 < 0.001 0.08 0.03 0.22 Sauced or cooked potatoes −1.66 0.66 0.011 0.19 0.05 0.68 White bread 1.03 0.36 0.015 2.38 1.18 4.78 Salta 0.91 0.42 0.052 2.27 0.99 5.21 Fruit drink −1.23 0.56 0.014 0.26 0.09 0.76

AOR = adjusted odds ratio; CI = confidence interval; SE = standard error.

The strength of this study was the Further studies are needed to clarify the range from 0.4 to 1.6 g per 100 g (29- comprehensiveness of the factors stud- effect of dietary factors and khat chew- 31). High salt intake is associated with ied. Besides, the numbers of cases and ing on gastric cancer and the mecha- H. pylori infection and is a promoter of controls were adequate for the statistical nisms involved in these processes, and gastric mucosal damage, hypergastri- power. However, the lack of important to improve food selection and cooking naemia and cell proliferation (32). This information on H. pylori infection could methods to prevent gastric cancer. result is consistent with another study limit the overall results. in Uruguay (13). In our study, intake In conclusion, the important risk of dairy products had an inverse sig- factors found in this study are modifi- Acknowledgements nificant association with gastric cancer, able, therefore, some recommendations which is supported by other studies (26, can be made to prevent gastric cancer. The authors would like to acknowledge 33). Nevertheless, these findings are The importance of health education the invaluable help given by data col- contrary to other studies in the Islamic and increased awareness of tobacco lectors, all workers in the National On- Republic of Iran (14, 24), and another chewing and risky dietary behaviour cology Centre, Sana’a City and all the study showed that dairy products had should be emphasized. Political action patients who participated in this study. no significant association with gastric is needed to curb tobacco consumption Funding: None. cancer (13). and improve water supply management. Competing interests: None declared.

References

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726 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Job satisfaction and its relationship to Radiation Protection Knowledge, Attitude and Practice (RP- KAP) of Iranian radiation workers S.S. Alavi 1, S.T. Dabbagh 2, M. Abbasi 1 and R. Mehrdad 1

الرضا الوظيفي وعالقته بمعلومات عامل األشعة اإليرانيني باحلامية من اإلشعاعات وباجتاهاهتم نحوها وبمامرستهم هلا سيدة شهره علوي، سيام تقي دباغ، حميا عبايس، رامني مهرداد اخلالصــة: هدفــتهــذه الدراســة إىل العثــور عــى العالقــة القائمــة بــني الرضــا الوظيفــي وبــني معلومــات الذيــنيتعرضــون لإلشــعاع املؤيــن من العاملــنييفجمــال األشــعة الطبيــة باحلاميــة مــن اإلشــعاعات وباجتاهاهتــم نحوهــا وبمامرســتهم هلــا وقــد قــام يف هــذه الدراســة املســتعرضة 530 عامــ ًال مــن عــامل األشــعة التابعــني جلامعــة طهــران للعلــوم الطبيــة بمــلء اســتبيان عــن املعلومــات واالجتاهــات واملامرســات املتعلقــة بحاميــة 2014 أنفســهم مــناإلشــعاع، وعــن َ ــب املنسالوصفــي للوظيفــة كمقيــاس للرضــا الوظيفــي مــن مايو/أيــار إىل نوفمرب/ترشيــن الثــاين مــن عــام . 91.5 84.2 فكانــت أهــم عوامــل االســتياء َالفــرص املتاحــة للرتقيــة )% ( والراتــب )% (. وكانــت مواقــف عــامل األشــعة املتزوجــني أكثــر إجيابيــة جتــاه محايــة أنفســهم مــن اإلشــعاع، واســتأثر املســتوى التعليمــي األعــى بـــ %15.8 مــن التبايــن الــكيل يف التنبــؤ بالرضــا الوظيفــي. ويف اخلتــام، فــإن عــامل األشــعة الطبيــة الذيــن كانــت اجتاهاهتــم جتــاه احلاميــة الذاتيــة مــن اإلشــعاع أكثــر إجيابيــة كانــوا أكثــر ًرضــا عــن وظائفهــم. ويمكــن اعتبــار حتســني مواقــف املوظفــ نيجتــاه ســالمتهم يف بيئــات اإلشــعاع اســرتاتيجية رئيســية لزيــادة الرضــا الوظيفــي.

ABSTRACT This study aimed to find the association between job satisfaction and radiation protection knowledge, attitude and practice of medical radiation workers occupationally exposed to ionizing radiation. In this cross- sectional study, 530 radiation workers affiliated to Tehran University of Medical Sciences completed a knowledge, attitude and practice questionnaire on protecting themselves against radiation and Job Descriptive Index as a job satisfaction measure during May to November 2014. Opportunities for promotion (84.2%) and payment (91.5%) were the most important factors for dissatisfaction. Radiation workers who were married, had more positive attitudes toward protecting themselves against radiation, and had higher level of education accounted for 15.8% of the total variance in predicting job satisfaction. In conclusion, medical radiation workers with a more positive attitude toward self-protection against radiation were more satisfied with their jobs. In radiation environments, improving staff attitudes toward their safety may be considered as a key strategy to increase job satisfaction.

Satisfaction au travail et lien avec les connaissances, attitudes et pratiques en matière de radioprotection des travailleurs iraniens exposés aux rayonnements

RÉSUMÉ La présente étude avait pour objectif de déterminer l’association entre la satisfaction au travail et les connaissances, attitudes et pratiques en matière de radioprotection des travailleurs exposés aux rayonnements médicaux ionisants dans le cadre de leur activité professionnelle. Au cours de cette étude transversale, 530 travailleurs exposés aux rayonnements rattachés à l’université de Sciences médicales de Téhéran ont rempli, entre mai et novembre 2014, un questionnaire portant sur les connaissances, attitudes et pratiques pour se protéger contre les rayonnements, ainsi que sur l’indice de satisfaction professionnelle Job Descriptive Index dans le but d’évaluer leur satisfaction au travail. Les possibilités de promotion (84,2 %) et les salaires (91,5 %) étaient les facteurs les plus importants d’insatisfaction. Les travailleurs exposés aux rayonnements qui étaient mariés étaient davantage disposés à se protéger des rayonnements, et avaient un niveau d’éducation plus élevé représentant 15,8 % de la variance totale relative à l’évaluation de la satisfaction au travail. En conclusion, les travailleurs exposés aux rayonnements médicaux ayant une attitude plus positive vis-à-vis du fait de se protéger étaient plus satisfaits de leur travail. Dans des environnements à rayonnement, améliorer la disposition du personnel à se protéger peut être considéré comme une stratégie clé pour augmenter la satisfaction au travail.

1Center for Research on Occupational Diseases, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran. 2Research Center for Science and Technology in Medicine, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran (Correspondence to: S.T. Dabbagh: [email protected]). Received: 06/08/15; accepted: 03/07/16 727 EMHJ • Vol. 22 No. 10 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

Introduction between job satisfaction and radiation including radiology or other fields in workers’ knowledge, attitude and prac- medical education, and participation Working with radiation can be haz- tice (KAP) regarding protecting them- in in-service training programmes over ardous if protective and preventive selves against radiation in the Islamic the past year. The second section was a measures are not observed and safety Republic of Iran and worldwide. There- modified version of the Job Descriptive regulations are not taken into account fore, the aim of the present study was Index (JDI) as a cognitive job satisfac- (1). The International Commission to analyse whether RP-KAP of Iranian tion measure, which was first developed on Radiological Protection (ICRP) as medical radiation workers can predict by Smith et al. (9). The JDI included 5 a primary body in protection against their level of job satisfaction. subscales: the nature of the work itself ionizing radiation classifies exposure (10 questions); attitudes towards su- in three categories: occupational expo- pervisors (8 questions); relations with sure including dose limits for radiation Methods co-workers (10 questions); opportuni- workers, public exposure, and medical ties for promotion (5 questions); and Study population and data payment (6 questions). All 39 questions exposure. According to the ICRP, so- collection cioeconomic factors are important for of the JDI were measured using 5-point limiting radiation exposure to as low as This cross-sectional survey was con- Likert scales from least (score 1) to reasonably achievable (2). In addition, ducted in Tehran University of Medical highest (score 5) occupational satisfac- socioeconomic factors are essential Sciences (TUMS), Islamic Republic tion. The score of each subscale and features of job satisfaction. A complex of Iran from May to November 2014. total job satisfaction for each participant interaction of several factors affects job All radiation workers in all 16 govern- were calculated by the following equa- satisfaction. Based on previous studies, mental referral hospitals affiliated to tions (9): TUMS, comprising physicians, nurses the most common factors include the Score of each subscale = and technologists, were asked to com- characteristics of the job, interaction Sum of scores of all items in each subscale with co-workers, immediate supervi- plete a comprehensive questionnaire Total number of items in each subscale sor, job promotion and salary (3). It anonymously. We used the census sam- seems that manipulating these variables pling method and one of the researchers Score of total job satisfaction = distributed the questionnaires by hand Sum of scores of all subscale may increase or decrease the level of Total number of items in each subscale job satisfaction among employees. Job at the workplaces of the participants. satisfaction can improve productivity Participants completed the question- Construct validity and reliability of and quality of life, reduce absenteeism, naires within a maximum of 12 minutes. the Iranian version of the JDI question- burnout and staff turnover, and improve In total, 530 of 720 questionnaires were naire (Cronbach’s α = 0.94) was already quality of patient care as well as occupa- returned, representing a response rate approved (10). tional safety (4). of 73.6%. The third section was a 32-item Medical radiation workers are ex- Participants gave written informed questionnaire consisting of 13 questions posed to low-dose ionizing radiation consent after receiving information to evaluate RP knowledge, 13 questions through multiple sources and this about the aims and protocol of the sur- about attitude and 6 questions related situation compromises their health and vey and they were assured regarding the to practice, developed based on the safety (5). Radiation protection (RP) confidentiality of their data. Participa- most common experiences and issues is one of the main factors that should tion in this study was voluntary and the that researchers encountered, as well as be considered to protect employees’ participants could stop the data collec- approved protocols and radiation safety health and safety (6). A major part of tion process at any time. The Medical guidelines. To evaluate content valid- health and safety protection at work is Ethics Committee of TUMS approved ity of the questionnaire, the content the core activities that employees need the research. validity ratio (CVR) and content valid- to carry out to maintain their own safety ity index (CVI) were used. Ten experts (7). Measures with different educational backgrounds Previous research has indicated that The research instrument was a self-ad- (including educational planning, epi- job satisfaction is affected by improving ministered questionnaire that included demiology, radiology and occupational skills and competencies of employees 3 sections. The first section was general health) assessed the questionnaire through participation in professional characteristics of the participants: sex, content in terms of asking the right development and career advancement, age, educational level, marital status, questions and avoid­ing ambiguity. The and by safety at work (8). Only a few years of experience working with ra- CVR of the questionnaire constructs studies have addressed the relationship diation, field of study at the university was 0.61–0.76 and CVI structure was

728 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

0.77–0.93. To measure the face validity degree (10.7%). The participants had a marital status, in-service training, field of the questionnaire, 30 radiation work- mean (SD) 9.2 (7.5) years experience of study, levels of education, years of ers and the 10 previously mentioned with radiation, and 335 (63.2%) had work experience with radiation, as well experts rated each question in terms of undertaken in-service training and 195 as RP-KAP to predict job satisfaction clarity, understandability and length of (36.8%) had not. (Table 4). Significant predictors includ- each question. Face validity was ensured Analysis of responses to each sub- ing positive attitude toward self-protec- by the revision of 7 items. To deter- scale of the JDI questionnaire indicated tion against radiation, higher levels of mine the reliability of the questionnaire, the levels of job satisfaction. A score of education and being married. TheR 2 of Cronbach’s α was calculated (0.92). To 1-3 represented low satisfaction and a the linear regression model was 0.158 determine participants’ level of KAP, a score of 3.1–5 high satisfaction. A high (F = 12.5, P < 0.001). Field of study numerical value was assigned to each percentage of participants, regardless (P = 0.013), in-service training during correct answer: knowledge (1.54), at- of profession, felt unsatisfied with the last year (P = 0.1) and years of experi- titude (1.54) and practice (3.33). The nature of their work (50.6%), their ence with radiation (P = 0.7) were not minimum and maximum scores were supervisors (41.5%), interaction with associated with job satisfaction. 0 and 20 for each set of RP-KAP ques- their colleagues (33.6%), opportunities tions. In this way, a score could be calcu- for promotion (84.2%), and payment lated for each participant in relation to (91.5%). More than half of respondents Discussion the highest possible score. (53.5%) perceived job dissatisfaction. The major focus of this study was an Data analysis General characteristics were not as- analysis of the link between radiation sociated with participants’ satisfaction All data was analysed using SPSS ver- workers’ job satisfaction and their with opportunities for promotion and RP-KAP about protecting themselves sion 21. We used descriptive statistics interaction with their colleagues (Table to describe our populations’ general against radiation in governmental refer- 1). Radiation workers with a degree in ral hospitals affiliated to TUMS. More characteristics. We compared quantita- radiology were less satisfied with their tive variables between two groups using than half of all radiation workers felt supervisors and nature of their work and total dissatisfaction. Consistent with the Mann–Whitney U test. We set total more satisfied with their payment. In job satisfaction as a dependent variable our study, Magnavita et al. (11) declared addition, there was no relationship be- that only 49% of diagnostic radiologists in a multiple linear logistic model to tween job training and subscales of job find predictors of higher job satisfaction were satisfied with their jobs. Another satisfaction, except attitudes towards study among oncology staff in radiation scores only for the significant factors supervisors (P = 0.04). in univariate analysis. Total job satis- oncology departments in New Zealand Radiation workers who had more faction was categorized into 2 levels: found a high level of job satisfaction years of experience with radiation were low satisfaction (scores 1–3) and high (3.75 mean score out of 5) (12). A 2013 significantly satisfied with their co- satisfaction (scores 3.1–5). study of Japanese radiologists reported workers (r = 0.14, P = 0.002), however, that 67.8% respondents were very or they were less satisfied with opportuni- somewhat satisfied with their current Results ties for promotion (r = 0.1, P = 0.03) job (13). Job satisfaction is a subjective (Table 2). and attitudinal issue that is influenced Five hundred and thirty radiation work- The relationship between self-rated by individuals’ wants, desires and many ers participated in this study. There RP-KAP and job satisfaction showed cultural and socioeconomic factors, so were 341 women (64.3%) and 189 that a more positive attitude toward self- it varies from person to person. Fur- men (35.7%), with a mean age (SD) protection was associated with higher thermore, measuring job satisfaction of 33.7 (15.7) years. Three hundred total job satisfaction (P < 0.001) and can be challenging and there is no gen- and forty-seven (65.5%) participants with all its subscales, including nature eral agreement on the best and standard were married and 183 (34.5%) were of the work (P < 0.001), interaction method of measurement. unmarried. Three hundred and twenty- with colleagues (P = 0.006), attitudes Among the 5 subscales of the JDI three (61%) had a degree in radiol- towards supervisors (P = 0.009), oppor- questionnaire, the highest level of dissat- ogy and 207 (39%) were other medical tunities for promotion (P = 0.017) and isfaction was observed for payment and specialists who worked professionally payment (P < 0.001) (Table 3). promotion. Other dissatisfiers, in order, with radiation. Level of education was: Additional linear logistic regression were the nature of the work, supervi- bachelor’s degree (70.6%), lower than was conducted to assess the ability of sors and co-workers. Previous research bachelor’s degree (18.7%) and higher significantly correlated factors such as about the most common dissatisfiers

729 EMHJ • Vol. 22 No. 10 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

support our findings 13( ). Our participants were more satisfied with interaction with their P

0.101 0.050 0.891 0.173 co-workers than the other subscales. In line < 0.001 with the present survey, another study showed that one of the most common sources of profes- sional satisfaction was the appreciation shown by radiologists’ supervisors and colleagues (14). Total job satisfactionTotal 3.0 (0.4) 3.0 (0.4) 3.0 (0.4) 3.0 (0.4) 3.0 (0.4) 3.2 2.9 (0.4) 2.9 (0.4) 2.9 (0.4) 2.9 (0.5) 2.9 (0.4) 2.9 (0.4) Mean (SD) Mean In the study of Graham et al. (15), one of the most important sources of job satisfaction was “being perceived to perform the duties properly P by co-workers”. Another study of job satisfac- 0.156 0.494 0.157 0.002

< 0.001 tion level among 8 healthcare profession groups indicated that radiation workers were more Payment satisfied in terms of supervision, co-workers,

2.3 (0.7) 2.2 (0.6) 2.2 (0.7) 2.2 (0.6) 2.3 (0.6) (0.7) 2.1 2.2 (0.7) 2.2 (0.6) (0.6) 2.1 2.2 (0.6) 2.5 (0.9) and the nature of the work (16). That study Mean (SD) Mean found significant differences in terms of sat-

P isfaction related to promotion, supervision,

0.135 0.754 0.392 0.098 0.003 co-workers and the nature of the work, but not in terms of payment. Our findings suggested that administrators could affect satisfaction Promotion by defining a reward system and ways to pay 2.4 (0.9) 2.4 2.2 (0.9) 2.3 (0.9) 2.2 (0.8) 2.3 (0.9) 2.3 (0.9) (0.9) 2.4 2.3 (0.9) (0.9) 2.4 2.2 (0.8) 2.7 (1.03) Mean (SD) Mean fair salaries, as well as facilitating job promo- tion for eligible radiation workers. Employers

P often have limited financial capacity to increase 0.239 0.053 0.092 0.600 0.001 salaries and their budget may not meet the satis- faction of all employees. However, promotions

Co-workers are not necessarily limited to pay increases and 3.4 (0.8) 3.4 3.3 (0.8) 3.3 (0.8) 3.4 (0.8) 3.3 (0.7) 3.4 (0.9) 3.3 (0.7) 3.4 (0.8) 3.4 (0.9) 3.5 (0.8) 3.3 (0.6) 3.7 can be awarded based on employees’ interests Mean (SD) Mean and values. Examples of promotion include offices with more advanced facilities and space; P 0.959 0.062 0.019 0.040 0.132 acknowledgement and positive feedback to perform a worthy activity; respect; highly valu- ing the position occupied by employees and Supervisors increasing authority over co-workers. Workers’ 3.2 (0.5) 3.2 (0.4) 3.1 (0.4) 3.2 (0.5) 3.1 (0.4) 3.1 (0.5) 3.2 (0.4) 3.2 (0.5) 3.1 (0.4) 3.2 (0.5) 3.2 (0.4) 3.3

Mean (SD) Mean expectation of job promotion has an important role in the effectiveness of promotion and in-

P creasing occupational satisfaction. In addition,

0.345 0.009 0.117 promotion may mitigate the impact of dissatis- < 0.001 < 0.001 faction caused by low payments resulting from Work the limited financial capacity of employers. In the present study, participants were more satis- 3.1 (0.6) 3.1 3.0 (0.5) 3.0 (0.5) 3.1 (0.5) 3.0 (0.5) 3.0 (0.6) 3.2 (0.5) 3.1 (0.6) 3.1 (0.5) 3.1 (0.5) 3.0 (0.5) 3.4

Mean (SD) Mean fied with their co-workers, supervisors and the nature of their work. It seems that these factors are harder to manipulate and require a large investment of time and money. Although most respondents were dissat- isfied in terms of payment, participants with a degree in radiology were more satisfied. In contrast, despite the high satisfaction in terms

Job satisfaction subscales of characteristics radiation general as regards workers of the nature of the work and supervisors

Male Female Married Unmarried Radiology Others Yes No thanLower Bachelor Bachelor Higher than Bachelor among all participants, respondents with a Characteristic Sex Marital status Field of study training In-service Level of education Table 1 Table degree in radiology reported less satisfaction.

730 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Table 2 Correlation of years of experiences with radiation and age with job satisfaction subscales Characteristic Work Supervisors Co-workers Promotion Payment Total job satisfaction r P r P r P r P r P r P Age (years) 0.02 0.7 0.05 0.2 0.09 0.06 −0.01 0.8 0.005 0.9 0.06 0.2 Experiences with radiation (years) 0.02 0.6 0.08 0.07 0.14 0.002 −0.10 0.03 0.04 0.3 0.07 0.1

A possible explanation is that gradu- was similar to previous studies (3, 17). that were not related to employees’ ates in radiology are interested in their In addition, in-service training was not main tasks might have underestimated jobs and low payments are tolerable. linked to total job satisfaction, which the worth of the most important per- However, they may have more infor- was also consistent with previous re- formance criteria, and consequently, mation about their workplace hazards, search (18). However, a previous study dissatisfaction might have increased. especially the potential risk of radiation reported that in-service training and Third, most of the training programmes exposure, and it seems they are more rewarding employees’ performance used ineffective methods that were not concerned regarding the nature of their and competence with promotion led to in accordance with employees’ learning job. Moreover, they expect supervisors greater job satisfaction (19). The lack of style. Therefore, in-service training did to try their best to mange workplace association between in-service training not attract participants. hazards where appropriate, control and total job satisfaction has several According to the regression analysis, the quality of equipment, and take re- possible explanations. First, healthcare job satisfaction and radiation workers’ sponsibility for occupational health and workers in the hospitals in our study attitude toward self-protection were safety. Therefore, dissatisfaction with were traditionally encouraged to par- associated. From practical and research work conditions and supervisors may ticipate in in-service training, which was perspectives, employees’ attitudes, opin- be more likely. neither perceived necessary by them ions and concepts regarding various as- Neither total job satisfaction nor nor planned based on their educational pects of their job and work environment its subscales were related to sex, which needs. Second, training programmes influence their job satisfaction 20( ).

Table 3 Self-rated RP-KAP based on participants’ job satisfaction Job satisfaction Knowledge Attitude Practice Mean (SD) P Mean (SD) P Mean (SD) P Work Low 6.8 (3.3) 8.0 (2.4) 11.9 (4.2) 0.109 < 0.001 0.003 High 7.4 (3.5) 9.4 (2.7) 13.0 (3.5) Supervisors Low 7.1 (3.5) 8.3 (2.7) 12.2 (4.4) 0.957 0.009 0.737 High 7.1 (3.4) 8.9 (2.6) 12.5 (3.6) Co-workers Low 6.8 (3.4) 8.2 (2.6) 11.6 (4.4) 0.333 0.006 0.004 High 7.2 (3.5) 8.9 (2.6) 12.8 (3.6) Promotion Low 7.1 (3.4) 8.5 (2.6) 12.4 (4.0) 0.778 0.017 0.815 High 7.2 (3.5) 9.3 (2.8) 12.3 (3.7) Payment Low 7.0 (3.4) 8.5 (2.6) 12.4 (4.0) 0.002 < 0.001 0.547 High 8.6 (3.4) 10.1 (2.8) 13.0 (3.5) Total job satisfaction Low 7.0 (3.5) 8.0 (2.5) 12.1 (4.2) 0.585 < 0.001 0.140 High 7.2 (3.4) 9.3 (2.7) 12.7 (3.6)

Low satisfaction = scores 1–3, high satisfaction = scores 3.1–5.

731 EMHJ • Vol. 22 No. 10 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

Table 4 Predictors of job satisfaction based on multiple linear logistic regression Variable B SE P OR 95% CI for OR Lower Upper RP Attitude 0.19 0.04 < 0.001 1.2 1.1 1.3 Marital status (married) −0.44 0.20 < 0.001 0.64 0.38 0.98 Level of education (higher than Bachelor’s) 0.39 0.10 < 0.001 1.48 1.18 1.85 Constant −3.3 0.9 < 0.001 – – – Total R2 0.158 F (P) 12.5 (< 0.001)

This is in line with previous research, safety leads to higher job satisfaction cases, try to cope with their job conflicts, which revealed that workers with higher (28). On the contrary, Hayes et al. have adjust them, or resolve any workplace safety perception expressed more job reported that management safety prac- problems. As a result, job satisfaction satisfaction compared to others (21). tices and supervisor safety subscales increases. Second, married employees Radiation is considered to be an exter- are good predictors of job satisfaction have opportunities to receive support or nal factor that contributes to difficult but workers’ safety is not (23). Another advice from their family to mediate job working conditions. Workers with dif- study investigating the link between job conflicts. The result can be increased job ficult working conditions have lower satisfaction and workers’ safety perfor- satisfaction. job satisfaction compared to those with mance has shown that workers with This study had some limitations. Job normal working conditions (22). Im- greater job satisfaction are often safer satisfaction has a subjective nature and provement of safety at work, providing workers. Conversely, safe workers are depends on employees’ wants, desires protective equipment and information, not necessarily satisfied 29( ). and opinions. Therefore, it varies from and urging employees to follow safety We found that higher level of educa- person to person and its predictors in rules and procedures ensure a safe work- tion was among 3 factors that predicted each society and organization are dif- ing environment, and reduce negative job satisfaction. This result was expected ficult to predict. Surveys such as ours attitudes toward safety and unnecessary because attaining a higher univer- assess a small set of potentially related fear and anxiety over radiation exposure. sity degree compared to lower degrees variables and can only provide manag- In this regard, workers who perceive contributes to a feeling of coherence, ers with specific information related to their workplace as safe experience lower success at work, personal growth and their own working environment. There- levels of occupational anxiety and face self-respect, self-realization and intrin- fore, there is no one-size-fits-all plan to fewer hazards (23). Further research sic motivation. The combination of all improve occupational satisfaction. In has revealed that job-related anxiety and these factors contributes to generating a this regard, it is noteworthy that, the low negative attitudes in the workplace are sense of job satisfaction. level of total R2 of the regression model among the variables that adversely cor- We found that marital status was assessing predictors of job satisfaction relate with the level of job satisfaction a predictor contributing to job satis- did not neutralize other significant (24). Therefore, improving attitudes of faction. The relationship between predictors. This means there are more radiation workers toward their safety these 2 variables has been extensively factors affecting job satisfaction and may be one of the effective strategies to investigated. However, there is contro- further research is needed to identify increase job satisfaction. versy about their relationship. In some them. In addition, job satisfaction is a Our findings showed that RP-KAP investigations, married employees ex- state of mind, so it is not a constant feel- did not predict job satisfaction. Previous perienced a higher level of job satisfac- ing. Assessment of its influencing factors studies have found that constant profes- tion than their unmarried co-workers and the magnitude of each one over sional development and improving staff (30), while in others, marital status time can provide organizations with capabilities in the workplace are princi- did not predict job satisfaction (31). clues to plan programmes in order to pal sources of job satisfaction (25,26). The positive relationship between the increase employees’ satisfaction. There- In addition, Abushaikha and Saca- 2 variables in the present study may fore, measuring job satisfaction using Hazboun have revealed that providing have several explanations. First, mar- longitudinal methods is more useful opportunities for professional develop- riage imposes certain responsibilities and recommended. Furthermore, it was ment increases job satisfaction (27). and makes a permanent job offer a top not possible to evaluate content, struc- Kaila has found that behaviour-based priority. Therefore, employees, in many ture and effectiveness of previous RP

732 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

training programmes. Interventional element. RP attitude, marital status and will encourage radiology managers and studies to assess the effectiveness of RP level of education were found to influ- administrators to find useful means to training programmes and their relation- ence job satisfaction. Future studies can improve radiation workers’ safety and ship with job satisfaction are recom- help to find other factors that influence job satisfaction in working lives. mended. job satisfaction and improve employ- Funding: This research was financially In conclusion, job dissatisfaction ees’ feelings regarding their work en- supported by the Vice-Chancellor for among medical radiation workers was vironment. It is hoped that this study Research of TUMS through contract high. Job satisfaction is multifaceted and will serve as an important platform for no. 93-02-109-25389. is influenced by more than just a single future detailed surveys and the findings Competing interests: None declared.

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734 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Turkish version of the SPAN questionnaire for high- school students: reproducibility and validity F. Öz 1, S. Metintas 1, R. Aydın 1 and Ö. Özay 1

النسخة الرتكية الستبيان النشاط البدين املدريس والتغذية اخلاص بطالب املدارس الثانوية: ُجالتنات واملصدوقية فاتح أوز، سلمى متني طاش، رشاد آيدن، أوزكان أوزاي اخلالصــة: هدفــت هــذه الدراســة إىل إجيــاد نســخة تركيــة الســتبيان النشــاط البــدين املــدريس والتغذيــة )2009( اخلــاص بطــاب املــدارس 318 الثانويــة وإىل اختبــار مصدوقيتــه وتناجتــه. ُفتجــم االســتبيان ثــم ُترجــم ًعكســيا ِّوقيمــت مصدوقيــة اللغــة. ُواختــر ُوأعيــد اختبــاره عــى ِ ً طالبــا مــنطــاب املــدارس الثانويــة لتقييــم مصدوقيتــه وتناجتــه. وقــد ُح ِّــددت مصدوقيتــهبمقارنــة أجــزاء االســتبيان املتعلقــة بــا ُأكل يف اليــوم الســابق مــع مــا هــو موجــود يف قوائــم اســتهلك الغــذاء عــى مــدار 24ســاعة. ثــم أجــري حتليــل إحصائــيباســتخدام حتليــل ارتبــاط ســبريمان وإحصائيــات كابــا والنســبة املئويــة للتوافــق. فكانــت أعــى نتائــج االختبــار وإعــادة االختبــار لألغذيــة املســتهلكة يف اليــوم الســابق، حيــث كانــت النســبة املئويــة للتوافــق تــراوح مــا بــني %56 و%96، وكابــا تــراوح مــا بــني 0.43 و0.95 وتــراوح التوافــق عــى البنــود املتعلقــة بالنشــاط البــدين مــا بــني %38 و%88، وتراوحــت كابــا مــا بــني 0.24 و0.82 إن تناتــج ومصدوقيــة النســخة التكيــة هلــذا االســتبيان مقبولــة، وهــي أداة رسيعــة ســهلة االســتخدام لتقييــم التغذيــة والنشــاط البــدين لــدى طــاب املــدارس.

ABSTRACT This study aimed to generate a Turkish version of the School Physical Activity and Nutrition (SPAN) (2009) questionnaire for high-school students and to test its validity and reproducibility. The questionnaire was translated and back translated and the language validity was assessed. It was tested and re-tested on 318 high- school students to evaluate its validity and reproducibility. Validity was determined by comparing the parts of the questionnaire about what was eaten in the previous day with that of 24-hour food consumption lists. Statistical analysis was performed by using Spearman correlation analysis, kappa statistics and percentage of agreement. The highest test−re-test results were on foods consumed the day before, with an agreement percentage range of 56%−96% and a kappa range of 0.43−0.95. The items related to physical activity had an agreement range of 38%−88% and a kappa range of 0.24−0.82. The reproducibility and validity of the Turkish version of SPAN questionnaire is acceptable and it is a rapid, easily used tool for the assessment of nutrition and physical activity in schoolchildren.

Version turque du questionnaire SPAN pour les élèves du secondaire : reproductibilité et validité

RÉSUMÉ La présente étude avait pour objectif de générer une version turque du questionnaire SPAN (School Physical Activity and Nutrition) [activité physique et nutrition en milieu scolaire (2009) pour les élèves du secondaire et de tester sa validité et sa reproductibilité. Le questionnaire a été traduit puis a fait l’objet d’une rétro-traduction, et la validité de la langue a été évaluée. Il a été testé puis re-testé sur 318 élèves du secondaire afin d’évaluer sa validité et sa reproductibilité. La validité a été déterminée en comparant les parties du questionnaire sur les aliments consommés le jour d’avant avec celle comprenant des listes relatives à la consommation alimentaire sur une durée de 24h. L’analyse statistique a été réalisée à l’aide de l’analyse de corrélation de Spearman, du test du kappa et du pourcentage de concordance. Les résultats test-retest les plus élevés concernaient les aliments consommés le jour d’avant, avec un pourcentage de concordance compris entre 56 % et 96 % et un coefficient kappa allant de 0,43 à 0,95. Les items liés à l’activité physique avaient un pourcentage de concordance de 38 à 88 % et un coefficient kappa de 0,24 à 0,82. La reproductibilité et la validité de la version turque du questionnaire SPAN est acceptable et constitue un outil rapide et simple d’utilisation pour évaluer la nutrition et l’activité physique chez les enfants scolarisés.

1Department of Public Health, Eskisehir Osmangazi University Medicine School, Eskişehir, Turkey (Correspondence to: F. Öz: ozzfatih@hotmail. com). Received: 05/06/14; accepted: 18/07/16

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Introduction Turkish to English linguists and the Testing the questionnaire language validity of the questionnaire The sample size for testing the question- Obesity in adolescents is a major prob- was assessed. Taking account of the so- naire was calculated to be 386 with a lem in developed as well as in devel- ciocultural norms in Turkey and some margin of error of 5% and considering oping countries (1). According to the other factors (e.g. religious, economic, the reliability of questionnaire as 50%. results of the HBSC (Health Behavıour climatic, access to enough food), a com- The questionnaire was tested among in School-Aged Chıldren) survey con- mittee of three experienced individuals 370 students out of 419 studying in ducted in Turkey, 14% of the males and (one epidemiologist, one medical doc- 1st or 2nd class of 4 high schools in the 5% of the females at age of 15 years in tor, one linguist) made some changes region of Sivrihisar located between 2001-2014) (5). It was stated in the in the questionnaires in order to as- the capital city Ankara and the city of action plan that interventions to address sure the cultural adaptation. For this Eskisehir in Central Anatolia Region. adolescent obesity require interactive purpose, the terms “hot dog and pig The 4 schools were elected by simple educational and behavioural support bacon” in 10th item were replaced by random sampling from the 8 regional regarding healthy eating and physical high schools with different educational “beef bacon and meat balls”, the term activity. The interventions themselves, programmes. as well as the measurability and ability “hot or cold cereal” in 33rd item was replaced by “corn flakes” and the “fro- The questionnaire was completed to monitor the interventions, have an by the students themselves under super- zen yoghurt-ice cream” was replaced by important role in the programme. The vision. The questionnaire was applied “cold sweet”. Items 39 (Last week, were ability to measure and monitor the in- during the school hours in the morning terventions allows the assessment of the the following available in your home?), from Tuesday to Friday because eating programme to be assessed. Therefore, 46 (How often does your family buy habits may change in the weekend. The surveillance tools should be available to or get fruits/vegetables from…) and re-test of “Did You Consume These monitor the eating habits and physical 50 [Do you use food labels (nutrition Foods Yesterday?” sub-section was ap- activity levels of the individuals. facts) to make your food choices?] in plied on the same day during the school School Physical Activity and Nu- the SPAN survey were not included in hours in afternoon, while the re-test of trition (SPAN-2009) questionnaire the Turkish version. These items were the other sub-sections was applied 7 was developed by the School-Based removed because these habits were only days after during the morning school Nutrition Monitoring (SBNM) pro- likely to apply to a small minority with hours. ject funded by the Centers for Disease high incomes in Turkey. Items 58 and A total of 52 students (14%) who Control and Prevention (CDC) and 59 were integrated and transformed were not at school at the time of study United States Department of Agricul- into one question as “How many teams or who gave incomplete or false infor- ture (USDA) and it is a well-accepted mation or who did not complete the surveillance tools. There are two forms did you play in during last year?” Finally, re-test were excluded from the study. of SPAN questionnaire developed for the items between 65 and 69 (questions The students excluded from the study using on primary and high school stu- about attitudes of parents towards their were those not completing more than dents (6). children) and between 81 and 91 (ques- 10% of the questionnaire and those who This study aimed to generate a tions about psychological situation) displayed deficient attention during the Turkish version of the SPAN (2009) were also excluded from the Turkish 20 minutes required to fill the question- questionnaire for high-school students version of the questionnaire. naire. and to test its validity and reproduc- The newly created Turkish version The 24-hour food consumption lists ibility. of the SPAN Questionnaire consisted were obtained following the 2-hour re- of 15 questions on sociodemographic test. Researchers followed a standard characteristics and 61 questions in six Methods dialogue with the students and recorded sub-sections (“Did You Consume foods on the 24-hour food consump- Translation of the SPAN These Foods Yesterday?”, “What foods/ tion lists. These lists were entered in the questionnaire meals do you usually consume?”, “Nutri- computer. The list of the foods eaten Permission from Deanna M. Hoelscher tion knowledge questions”, “Nutrition the previous day was adapted from the was received to generate the Turkish attitude questions”, “Weight behaviour foods included in the SPAN food con- version of SPAN-questionnaire. The questions” and “Physical activity ques- sumption questionnaire. The students questionnaire was translated and back tions”). In total the survey consisted of reporting calorie intake of less than 500 translated by English to Turkish and 76 questions. kcal or more than 5000 kcal in 24 hours

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were also excluded since these were agreement were used to assess the 24- agreement and kappa coefficient for highly improbable intakes and were hour food consumption list and test−re- this part ranged from 61% to 93% and likely incorrect. Students’ self-reported test agreement for each item. from 0.46 to 0.91 respectively (Table height and weight were recorded. Body Overall, the level of compliance 1). The items with the highest agree- Mass Index (BMI) was calculated and indicated by the Spearman correlation ment percentage and kappa coefficient reference norms published by WHO coefficient ranges as follows: < 0.20 were the eating “fried chicken-fish” and were used (7,8). weak; 0.20−0.39 low; 0.40−0.59 moder- “dining out”, although the latter did not have a high kappa value, while those Ethical clearance ate; 0.60−0.80 high; and > 0.80 strong relationship. The kappa statistic is used with lowest were eating a “snack” and Eskisehir Osmangazi University to examine the agreement between the “consuming chocolate”. The Spearman Medical Faculty Non Drug Clinical test and re-test scores for each item. correlation coefficient ranged from 0.40 Research Ethical Committee approved This statistical method yields reliable to 0.84, the highest being for the item the study (ethical committee report: statistical data in terms of eliminating “nuts” (0.84) and lowest for the item 80558721/244). All necessary permis- the effect of chance. The level of com- “orange-coloured vegetables” (0.40). sions from the institutions and oral pliance indicated by kappa coefficient For the questions related to the informed consent from all participants ranges as follows: < 0.20 inadequate; consumption of fruits and vegetables, was obtained. 0.21−0.40 weak; 0.41−0.60 moderate; the Spearman correlation coefficient Data analysis 0.61−0.80 strong; and 0.81−1.00 excel- showed moderate reliability, while lent compliance. The kappa statistic agreement percentages and kappa coef- Data were analysed with SPSS, version and adjusted kappa statistic, adjusted ficients showed high reliability. 15.0. There is no consensus in the litera- ture about the best method of statisti- for the extraordinary variables, were Because mean correlation did not cal analysis to assess the reliability and determined using pre-prepared tables differ between females and males, the validity of estimating if the nutrition at: http://vassarstats.net/kappa.html. results shown in tables were given for is good or bad. Spearman correlation Agreement percentage was calcu- the whole study sample. coefficient, kappa coefficient and the lated as the percentage giving the same The validity assessment of the percentage of agreement were used answer to the same question both in the questionnaire was performed only because of nonparametric data (9). test and re-test (10). for the part “Did you consume these The analysis was performed in two- foods yesterday?” (Table 1). For this steps. In the first step assessing the valid- purpose, the 24-hour food consump- ity, the 24-hour food consumption lists Results tion lists converted into comparable were compared with the list in the SPAN data with SPAN results. The agreement The study group consisted of 318 stu- questionnaire on the foods consumed percentage and kappa statistic ranged dents in the age group of 14−15 years, the previous day. In the second step, the from 56% to 98% and from 0.43 to with a mean age and standard devia- “Did You Consume These Foods Yes- 0.95 respectively. The first five items tion (SD) of 14.7 (SD 0.5) years. There terday?” sub-section of the question- with highest values in both analyses naire was assessed by calculating the were slightly more girls [168 (52.8%)] included “fruit juice”, “dining out” and internal consistency, Cronbach α and than boys. Based on BMI, 55 (17.2%) “cornflakes consumption” in common intraclass correlation coefficient. The students were overweight or obese. and those with lowest values included Cronbach α of 0.40−0.60, 0.60−0.80 The Cronbach α intraclass correla- “snacks”, “rice-pasta consumption” and and > 0.80 indicates low, moderate or tion coefficient was 0.71 for the ques- “tea-coffee consumption” in common. high reliability for the questionnaire tion of “Did you consume these foods The Spearman correlation coefficient respectively. yesterday?” ranged from 0.11 to 0.89, being highest Because the other sub-sections con- The reproducibility with the ques- for the item “fruit juice” (0.89) and low- sisted of very heterogeneous answers, tion “Did you consume these foods est for the item “snacks” (0.11). the Cronbach α test was not performed. yesterday?” and validity analysis with The reproducibility analysis for the Spearman correlation coefficient, kappa the 24-hour food consumption lists are items related to usual food consump- coefficient and the percentage of agree- shown in Table 1. tion and the nutritional knowledge and ment were used for reliability for these The highest results in the test−re-test attitudes is show in Table 2. sub-sections. comparison was in the part including The agreement percentage and Spearman correlation coefficient, questions of “Did you consume these kappa coefficient for the items of “What kappa coefficient and the percentage of foods yesterday?” The percentage of foods/meals do you usually consume?”

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Table 1 Reproducibility of the Turkish SPAN questionnaire by the question “Did you consume any of these foods yesterday?” and validity analysis by the 24-hour food consumption lists Food and meal choice behaviour Test- Validity analysis by the 24-hour food questions: “Did you consume consumption these foods yesterday?” Correlation Kappa Agreement (%) Correlation Kappa Agreement (%)

Meat (hamburger, meatballs, ribs) 0.69 0.82ª 85 0.78 0.78 96 Fried chicken or fish 0.70 0.91ª 93 0.88 0.87 98 Nuts (peanuts, walnuts, almonds …) 0.84 0.71 81 0.62 0.80ª 84 Any kind of cheese 0.79 0.64 78 0.73 0.71ª 76 Any kind of milk 0.65 0.73ª 78 0.63 0.88ª 90 Yoghurt and yoghurt drink 0.83 0.691 80 0.55 0.57 76 Rice, macaroni or pasta noodles 0.74 0.65 75 0.65 0.43ª 62 White bread, buns, bagels 0.62 0.52 67 0.51 0.48 66 Whole wheat or dark bread 0.65 0.90ª 91 0.39 0.88ª 92 Cereals 0.64 0.84ª 87 0.74 0.95ª 96 French fries or chips 0.73 0.62 80 0.67 0.66 84 Any starchy vegetables (potatoes, 0.48 0.67ª 72 0.60 0.76ª 80 corn, peas …) Any orange vegetables (carrots, 0.40 0.75ª 80 0.74 0.76 94 sweet potatoes) A salad with any green vegetables 0.80 0.69 79 0.84 0.61 74 Any other vegetables (tomatoes, 0.67 0.53 69 0.31 0.59ª 66 peppers, zucchini) Any kind of beans 0.58 0.80ª 83 0.71 0.77 94 Fruits (fresh, frozen, canned or 0.43 0.73ª 78 0.36 0.66ª 72 dried fruits) Fruit juice (freshly squeezed) 0.72 0.87ª 89 0.89 0.91 98 Any soft drinks 0.74 0.61 74 0.52 0.61ª 68 Any diet soft drinks 0.64 0.87ª 89 0.57 0.63 82 Water 0.83 0.72 81 0.48 0.59ª 66 Coffee, tea, ice tea 0.69 0.53 67 0.41 0.47 66 Frozen dessert 0.62 0.86ª 88 0.83 0.84 98 Sweet rolls, doughnuts, cookies … 0.62 0.69ª 75 0.53 0.68ª 74

Any candy, chocolate 0.72 0.51 65 0.44 0.61a 68 Eating any type of restaurant(fast 0.58 0.59 92 0.85 0.95a 96 food, pizza places, coffee shops) Snacks 0.60 0.46 61 0.11 0.47a 56 Number of meals 0.60 0.76a 80 0.42 0.68a 74

aAdjusted kappa statistic.

ranged from 53% to 89% and from 0.39 coefficient and Spearman correlation The agreement percentage, kappa to 0.84 respectively. The highest and coefficient, with ranging from 46% to coefficient and Spearman correlation lowest values common in both analysis 73%, from 0.33 to 0.59 and from 0.19 coefficient for the items about nutri- were for “vitamin-mineral intake” and to 0.33 respectively (Table 2). Among tional attitudes ranged from 46% to “type of milk”, respectively. The Spear- these items, the highest result was ob- 55%, from 0.29 to 0.41 and from 0.25 to man correlation coefficient ranged be- tained for “If I am overweight I am more 0.48 respectively. The rank of the items tween 0.25 and 0.52. likely to have more health problems was similar in all three analyses. The part of questionnaire about nu- like cancer or heart disease”, while the The agreement percentage, kappa tritional knowledge and attitudes had lowest result was for “How many total coefficient and Spearman correlation the lowest agreement percentage, kappa cups of fruits should you eat each day?” coefficient for the weight behaviour

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Table 2 Reproducibility analysis for the items related to nutritional knowledge and attitudes Description of questions Test- Correlation Kappa Agreement (%) Food and meal choice behaviour “What foods/meals do you usually consume?” questions Vitamins and minerals supplementation 0.25 0.84a 89 Type of milk 0.47 0.39 53 Eat breakfast 0.48 0.48a 61 Eat school lunch 0.52 0.54 69 Eat dinner 0.29 0.84a 85 Nutrition knowledge questions Servings of fruit in a day 0.19 0.33a 46 Servings of vegetables in a day 0.31 0.41a 53 Highest calorie contents 0.33 0.37a 53 Diet and chance of heart disease, cancer 0.33 0.59a 73 Nutrition attitude questions I eat healthily, no reason to make changes 0.25 0.29a 46 Healthy foods taste good 0.33 0.32a 49 Help prepare meals at home 0.48 0.41a 55 Weight behaviour questions Have you ever tried to lose weight? 0.48 0.63a 75 Weight preference 0.48 0.41 58 Weight compared with peers: too much, too little, about right 0.34 0.50a 66 Physical activity questions Current participation in organized physical activities 0.33 0.61a 74 Recommended minutes of physically activity 0.36 0.29 45 Number of hours of television watching per day 0.45 0.24 38 Number of hours of video game playing per day 0.35 0.43a 50 Days of walking or bicycling, 60 min. in past 7 days 0.79 0.63 68 Days of exercise with heart fast/breath hard, 20 min, past 7 days 0.82 0.65 76 Days of exercise to strengthen or tone muscles, past 7 days 0.85 0.69 82 Numbers of team sports, past 12 months 0.86 0.82 88

aAdjusted Kappa statistic.

items ranged from 66% to 75%, from questions in terms of reproducibility consistency coefficient, the higher con- 0.41 to 0.63 and from 0.34 to 0.48 re- and validity. sistency between the items. The second spectively. The rank of the items was criterion is the consistency between also similar in all three analyses. the results obtained at different time Discussion points, which is assessed by the test−re- The agreement percentage, kappa test method. The test−re-test reliabil- coefficient and Spearman correlation Reliability is defined as the extent to ity analysis assesses the tool in terms of coefficient for items about physical -ac which a measurement tool measures consistency of results on repeated uses tivity ranged from 38% to 88%, from the intended feature and the ability to produce consistent results. There are and invariability with the time. For this 0.24 to 0.82 and from 0.33 to 0.86 purpose, the questionnaire is re-applied respectively. The scores on the items two main criteria for the assessment of the reliability of a tool. The first one is some time after the period of initial ap- related to exercises were better than the consistency between the responses plication (11). those related to the inactive time spent. obtained at the same time. The reli- Overall, the test−re-test reliability No significant gender and BMI dif- ability coefficient, Cronbach α is used for the question of “Did you consume ferences were detected for any survey for this purpose. The higher the internal these foods yesterday?” was found to

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be good. The Kappa and Spearman cor- foods (15). On the other hand, because such as asking about the foods eaten the relation coefficients were higher in less the translated SPAN questionnaire has previous day, so students may have had frequently consumed foods. Because a Cronbach α coefficient of 0.71 with difficulty in remembering these foods, it is possible that the frequently con- an acceptable reliability and because resulting in the underestimation of reli- sumed foods could not be stated as the the part of the questionnaire assess- ability. Hoelscher et al. also reported exact number of daily consumption, ing foods eaten the previous day has similar results in their study (12). the reliability might be underestimated. the properties of other existing scales, Although the reproducibility of the Furthermore, the low reliability of the the translated SPAN questionnaire can weight behaviour items and physical items related to vegetables might be be considered appropriate for using in activity items was at a moderate level, due to the difficulty in remembering the epidemiological studies on the nutri- it was better than that of nutritional vegetables in mixed foods. Hoelscher et tional habits of adolescents in Turkey. knowledge and attitudes items. The low al. have also reported low reliability for Furthermore, the SPAN questionnaire reproducibility found for the physical frequently consumed foods and high has been reported to be a rapid and activity items assessing the inactive time reliability for less frequently consumed easily used measurement tool for the spent might be a result the students hav- foods (12). Thiagarajah and colleagues assessment of nutrition in school classes ing difficulty in remembering the time have also reported similar results (13). (12,13,16). they have spent inactively. Hoelscher The results of present study revealed The lowest reliability was found for et al. reported an acceptable level of no difference in reproducibility between the item about the “type of milk” among reliability for the items about physical the males and females. There are other the items of “What foods/meals do you activity (12). previous studies reporting no differ- usually consume?” According to the There are a few limitations with re- ence in reproducibility and validity of data from National Dairy Council, 45% gard to the SPAN questionnaire and the questions about food consumption of the milk produced in Turkey is raw our Turkish version. Because the part of frequency in terms of gender (12,13). milk, compared to under 1% in the Unit- the SPAN questionnaire assessing the The validity of the items within “Did ed States of America (17). As a result, eating habits in the previous day meas- you consume these foods yesterday?” the reproducibility for the “type of milk ures just one day, it does not represent assessed by the 24-hour nutritional consumed” might be underestimated the overall food consumption. Further- consumption list was found to be good due to the fact that many individuals more, the questionnaire is appropriate overall. The low validity for the items were consuming raw milk. So raw milk for the evaluation of groups rather than “snacks” and “tea-coffee consumption” could be added to the Turkish version individuals. Finally, because the Turk- might have resulted from difficulty in of SPAN questionnaire. Furthermore, ish version was used on students in a remembering how many times these the low reliability might be due to the limited region, the findings may not rep- foods are eaten/drunk due to their fact that milk is usually bought by the resent the whole geographical region of frequent consumption. Furthermore, parents and that children are not usu- Turkey and needs to be tested on larger snacks might not be considered as a ally concerned about the type of milk and different samples. food by some individuals. Thiagarajah bought or consumed. Thiagarajah and and colleagues also reported low valid- colleagues also reported that students ity for the frequently consumed foods had difficulty in remembering what Conclusions (13). kind of milk they were consuming (13). In Turkey, there are a limited num- In the present study, the part includ- The Turkish SPAN questionnaire was ber of validity and reliability studies for ing items about nutritional knowledge found to be a rapid, easily used and the nutrition in adolescents. The study and attitudes had the lowest reproduc- reproducible tool for the assessment conducted by Demirezen et al. used a ibility. It might be that the students were of nutrition and physical activity in 5-point Likert scale including the state- interested in the questions about nutri- schools. However, it should be used ments ranging from “never” to “always” tional knowledge and tried to learn the on larger and different study samples for the assessment of food consumption correct answers, which may have led to repeatedly in order to obtain additional (14). Arikan et al. used the translated the inconsistency in the reproducibility data about the reliability and validity of scale of the “Adolescent Food Habit of items about nutritional knowledge. the questionnaire. Checklist”, which assessed the amount Furthermore the items about attitudes Funding: None. and frequency of the consumption of included no specified time interval, Competing interests: None declared.

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741 EMHJ • Vol. 22 No. 10 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

Knowledge of diabetes among patients in the United Arab Emirates and trends since 2001: a study using the Michigan Diabetes Knowledge Test M. Jawad Hashim 1, H. Mustafa 1 and H. Ali 2

معلومــات املــرىض عــن الســكري يف اإلمــارات العربيــة املتحــدة منــذ عــام 2001: دراســة باســتخدام اختبــار ميتشــيجان للمعلومــات املتعلقــة بالســكري حممد جواد هاشم، هالة مصطفى، حبيبة عيل اخلالصــة :إن املعرفــة بمــرض الســكرى لــدى املــرىض ىف االمــارات العربيــة املتحــدة عامــل اساســى للرعايــة الذاتيــة. لقــد قيمنــا مســتوى املعرفــة عنــد مــرىض الســكرى ىف دراســة مقارنــة مــع دراســات ســابقة ىف نفــس املدينــة. اجرينــا دراســة مقطعيــة مســتخدمني اســتبيان جيــرى بواســطة مقابــات ىف عيادتــ نيىف منطقــة العــني، االمــارات العربيــة املتحــدة. اســتخدمت النســخة املرتمجــة الختبــار ميتشــجان لتقييــم مــدى املعرفــة ملــرض الســكرى. مــن اصــل 165 مشــارك مصــاب بالســكرى كان عــدد النســاء 130 )%78.8(. إن متوســط الدرجــات املحــرزة للمعرفــة كان منخفضــا اىل %55 )6.6 مــن 12 وهــى اعــى درجــة ممكــن احرازهــا، االنحــراف املعيــارى 1.8(. وهــذا املســتوى مشــابه للمســتويات التــى وجــدت ىف دراســات ســابقة % 55.5ىف عــام 2001 و % 68.2ىف عــام 2006. إن املفاهيــم اخلاطئــة حــول النظــام الغذائــى وفحــص الــدم ملــرض الســكرى تعتــر شــائعة. وقــد ظــل مســتوى املعرفــة بمــرض الســكرى متدنــى منــذ عــام .2001 إن هــذه النتائــج تبعــث عــى القلــق بالنظــر اىل حجــم االســتثامرات الكبــرة التــى وظفــت ىف جمــال مــرض الســكرى والتثقيــف الصحــى ىف املنطقــة.

ABSTRACT Knowledge of diabetes among patients with the disease in the United Arab Emirates is essential for effective self-management. We assessed the level of diabetes-related knowledge among patients and compared it with that found in previous studies in the same city. A cross-sectional study, using an interviewer-administered questionnaire, was conducted at two clinics in Al Ain, United Arab Emirates. The Michigan Diabetes Knowledge Test, translated into Arabic, was used to assess knowledge of diabetes. Of 165 participants with diabetes, 130 (78.8%) were women. The mean knowledge score was low at 55% (6.6 out of a maximum possible score of 12, standard deviation 1.8). This is comparable to levels found in previous studies: 55.5% in 2001 and 68.2% in 2006. Misconceptions about the diabetic diet and blood testing were common. The level of diabetes-related knowledge has remained low since 2001. These results are of concern in view of the substantial investments made in diabetes care and health education in the region.

Connaissance du diabète parmi les patients aux Émirats arabes unis depuis 2001 : étude menée à l’aide du test d'évaluation des connaissances sur le diabète du Michigan

RÉSUMÉ La connaissance du diabète parmi les patients atteints de la maladie aux Émirats arabes unis est essentielle pour une auto-prise en charge efficace. Nous avons évalué le niveau de connaissance sur le diabète parmi les patients et l’avons comparé avec celui trouvé dans les études précédentes menées dans la même ville. Une étude transversale, reposant sur un questionnaire administré par un enquêteur, a été conduite dans deux cliniques à Al Ain, aux Émirats arabes unis. Le test d'évaluation des connaissances sur le diabète du Michigan, traduit en arabe, a été utilisé pour évaluer la connaissance du diabète. Sur 165 participants diabétiques, 130 (78,8 %) étaient des femmes. Le score de connaissance moyen était bas (55 %, soit 6,6 sur un score maximum possible de 12, avec un écart-type de 1,8). Ceci est comparable aux taux trouvés dans les études précédentes : 55,5 % en 2001, et 68,2 % en 2006. Des idées reçues sur le régime alimentaire pour diabétiques et les analyses de sang étaient courantes. Le niveau de connaissance sur le diabète reste bas depuis 2001. Ces résultats sont préoccupants compte tenu de l’investissement non négligeable réalisé dans le domaine des soins apportés aux patients diabétiques et de l’éducation sur le diabète dans la région.

1Department of Family Medicine, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates (correspondence to: M. Jawad Hashim: [email protected]). 2Department of Nutrition and Health, College of Food and Agriculture, United Arab Emirates University, Al Ain, United Arab Emirates. Received: 04/15/15; accepted: 04/08/16 742 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Introduction investments in health systems on Data collection instrument diabetes knowledge among the diabetic We used the Michigan Diabetes Knowl- Knowledge about diabetes among patients in the city of Al Ain, the fourth- edge Test (MDKT) (13), with adapta- patients is considered critical for good largest metropolitan area in the UAE. tions as described below. The MDKT is self-management (1). While diabetes- The objective of this study, therefore, a validated instrument with fairly good related knowledge is generally associ- was to assess the changes in diabetes- reliability (alpha = 0.71) (13), and has ated with better glycaemic control (2), related knowledge among patients with been widely used in different settings this is not always the case (3). Still, pa- diabetes in Al Ain, in comparison with to assess knowledge of diabetes among tients who have knowledge of diabetes the previous studies. patients (8, 14-16). The online ques- are likely to have fewer misconceptions tionnaire in English (17) has 14 items and a better understanding of the health that assess knowledge of diabetes and consequences of the disease (4). Methods nine items that evaluate understanding In the Eastern Mediterranean Re- of insulin use. Each item is structured as gion, the burden of diabetes contin- A cross-sectional study was conducted a question with a single correct answer, ues to increase (5). Researchers have using an interviewer-administered and three or four answer options are stressed the urgent need for education pre-validated questionnaire to assess given. The questionnaire items deal with on diabetes and nutrition (6). In one knowledge of diabetes among adult diet, blood glucose control and compli- study, over one-quarter of the patients Emirati Arab patients with type 2 cations of diabetes. with diabetes could not recognize or diabetes mellitus. The study was con- We adapted the MDKT as follows. respond to the symptoms of hypogly- ducted from February to June 2014 at A bilingual researcher (HM) translated caemia, even though many of them the items into Arabic in several iterations, two clinics affiliated with a tertiary care were taking insulin (7). In a group of checking for consistency and idiomatic hospital in Al Ain city. Both clinics have Arab women with gestational diabe- expression of the original meaning. diabetes nurse educators and dieticians, tes, knowledge was not better than in a Some of the answer options were control group of non-diabetic women and treat patients with diabetes using modified to be more locally relevant. In (6). Importantly, in Arab patients with a chronic disease care model and an item 2, “Swiss cheese” was changed to diabetes, disease-related knowledge electronic health record system. Writ- “haloumi cheese” (a local variety), and was found to be correlated with better ten informed consent was obtained “peanut butter” to harees“ ” (a traditional adherence to medication (8). from study participants after the intent Arabic dish made from whole wheat The United Arab Emirates (UAE) is and process of the research had been and chicken or meat). Similarly, in item experiencing a transition, in which rapid explained. A trained medical research 3, “corn” was changed to “boiled rice”. socioeconomic development has led assistant carried out the interviews using In item 5, “day” was replaced by “one to an epidemic of obesity and diabetes. paper forms for data collection. month”, and “6–10 weeks” was changed Studies of diabetes prevalence place the to “3 months”. In item 6, “both equally UAE among the regions with the high- Eligibility criteria and methods good” was replaced by “how I feel”. The est burden of disease, with an estimated of participant selection original question in item 8 was in a nega- 29.0% of adults aged 30–64 years hav- The eligibility criteria were: age more tive format (“should not be used”); this ing diagnosed or undiagnosed diabetes than 18 years, Emirati Arab ethnicity was changed to a positive form (“should (9). Additionally, high burdens of pre- (stipulated by the funding agency), and be used”), and the following answer op- diabetes (22.7%) and obesity (37.3%) a diagnosis of type 2 diabetes mellitus. tions were given: three pieces of candy, were found in a community survey in Patients with diabetes mellitus type eating carrots, one cup of diet soda, and the city of Al Ain, which continue to eating popcorn. Finally, for item 11, 1 were excluded, as were those with fuel the diabetes epidemic (10). This is “massage with alcohol” (rarely used any apparent mental, visual or hearing of concern, since only 41% of Emirati in the region) was changed to “apply impairment. Participants were selected patients at a dedicated diabetes centre moisturizing cream daily”. An earlier in Al Ain achieved their glycaemic con- using non-random sampling in the wait- study (12) in this region reported mak- trol goals (11). Cross-sectional studies ing areas of the clinics. After obtaining ing similar changes with regard to local of diabetes knowledge among patients approval from the clinic nurse in charge, foods. The changes did not alter the cor- were conducted by the United Arab the research assistant approached po- rect answers. Item 4 was omitted, as the Emirates University in 2001 and 2006 tential participants in the clinic waiting use of the phrase “free food” is uncom- (3, 12). These now provide an oppor- areas. Those who gave consent were mon in our region and the question was tunity to assess the impact of intensive interviewed in a private area. difficult to interpret after translation.

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Similarly, item 9 on the effect of exercise analyse the data and conduct bivariate in clinics in this region. The level of dia- on blood glucose was felt to be unclear correlations, analysis of variance tests betes knowledge was low, as indicated for local use and was removed. The nine (two-sided testing with significance by the mean number of correct answers items related to insulin use were not level preset at 0.05) and multiple linear to the 12 questions: 6.6 (55% correct incorporated in our study, since most regression. Quantitative data (continu- responses), standard deviation (SD) potential participants were not being ous variables) were not grouped prior to 1.8. Using an arbitrary cut-off point of 6 treated with insulin. statistical analysis. Missing values were correct answers as a minimum satisfac- not imputed. At the end of data col- tory level, 41 participants (24.8%) were Other variables lection, age and year of diagnosis were below this level. We collected self-reported demograph- missing for 10% and 32% of patients, respectively. However, almost all the Responses to specific ic data on participants, including age, questions sex, educational attainment, and years MDKT questionnaire items had com- Figure 1 shows the answers to some since diagnosis of diabetes. For some plete data. No adjustments were made of the questions. Reassuringly, most patients, an attendant, usually a family to the analysis, as the sampling strategy participants were aware that the diabetic member or a domestic aide, assisted in yielded fairly representative data. diet is a healthy diet, and knew about answering these questions. We reduced diabetes complications. However, 92 bias in our data by using the same inter- Results (55%) thought that harees was higher viewer and questionnaire throughout in carbohydrates than baked potatoes, the study. Table 1 presents the demographic and 80 (49%) were under the impres- A minimum sample size of 150 characteristics of the 165 participants. sion that boiled rice had more fat than subjects was needed to differentiate Most of the participants were older low-fat milk. Misconceptions about between scores of 0.50 and 0.65 with a patients, women, or persons with newly haemoglobin A1c and urine glucose power of 95% and alpha level of 0.05. diagnosed diabetes; this is consistent tests were also not uncommon. Perhaps SPSS software version 21 was used to with patient patterns generally observed of greater concern are the incorrect

Table 1 Characteristics of the 165 study participants Characteristic Number of participants (%) Mean test scorea Significanceb (SD) (P value) Age (years) 0.004 ≤ 30 5 (3.0) 6.0 (2.0) 31–40 16 (9.7) 6.9 (1.5) 41–50 52 (31.5) 7.3 (1.5) 51–60 58 (35.2) 6.1 (1.9) ≥ 61 18 (10.9) 5.9 (2.0) Sex 0.602 Male 20 (12.1) 6.8 (1.4) Female 130 (78.8) 6.6 (1.9) Educational attainment 0.039 No schooling 38 (23.0) 5.9 (1.8) Primary school 11 (6.7) 7.2 (1.7) Junior school 3 (1.8) 5.7 (1.5) Senior school 75 (45.5) 6.8 (1.8) College graduate 23 (13.9) 7.0 (1.6) Number of years since 0.896 diagnosis of diabetes ≤ 5 73 (44.2) 6.9 (1.8) 6–10 37 (22.4) 6.9 (1.8) ≥ 11 3 (1.8) 7.3 (0.6)

a Out of 12 questions. b One-way analysis of variance of test scores.

744 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

12. Low fat food prevents: heart disease

1. Diabetic diet: a healthy diet

14. Diabetes complications do not include: lung disease

11. Foot care: look and wash daily

13. Tingling and numbness are a sign of: nerve disease

5. Haemoglobin A1c duration: 3 months

7. Effect of unsweetened fruit juice: raise blood glucose

2. Highest in carbohydrate: baked potato

3. Highest in fat: low-fat milk

6. Best glucose test: blood test

0 25 50 75 100

% of respondents (N=165)

Figure 1 Percentage of participants responding correctly to selected questions

answers for treating hypoglycaemic epi- no schooling to 7.0 among those with patients has remained low and relatively sodes (not shown in Figure 1): only 105 college education (P = 0.039; one-way unchanged over 14 years is disconcert- (64%) thought that sweets should be analysis of variance (ANOVA)). Inter- ing, especially in view of major invest- used, while the rest chose inappropriate estingly, the diabetes knowledge score ments in health care in general and options such as popcorn or diet soda. was similar among male and female diabetes care in particular. Furthermore, 61 (37%) gave medically participants (P = 0.602). On multiple There may be several possible ex- inappropriate responses to the ques- linear regression, none of the covari- planations for these results. The rapidly tion about foot care, indicating a lack of ables (age, sex, years since diagnosis and rising prevalence of diabetes may have awareness and patient education. educational attainment) were statisti- outstripped the ability of the health cally significant predictors of the overall system to provide adequate health edu- Diabetes knowledge and age 2 score (R = 0.011). cation. A shortage of health care profes- The correlation analysis showed that sionals, especially diabetes educators, diabetes knowledge tended to decrease Trend analysis may be a contributing factor. Diabetes slightly with age (R = -0.196, P = 0.017). Comparison of the results of the present knowledge appears to depend partly Unexpectedly, the knowledge score did study with the baseline data from the on the availability of structured educa- not increase with the number of years earlier studies revealed no improve- tion programmes at health facilities, since diagnosis (R = 0.026, P = 0.79). As ment in diabetes knowledge scores in and not on other system factors, such might be expected, participants’ age was patients in Al Ain (Figure 2). correlated with years since diagnosis (R as the speciality of the caring physician = 0.52, P < 0.0001). (18). Health systems development may Discussion not yet be fully adapted to the chronic Diabetes knowledge and care model. Care processes for effec- educational attainment Two previous studies using the MDKT tive management of chronic disease are Diabetes knowledge scores were higher questionnaire in clinic settings in Al often difficult to implement, leading to among participants with more years Ain city, in 2001 and 2006, observed episode-based care delivery (19). Addi- of education, although the difference low levels of knowledge about diabetes tionally, health education is a challenge was small. The scores ranged from a among patients. Our study’s finding in multicultural societies and among mean of 5.8 among participants with that the level of diabetes knowledge in groups with low literacy rates. Yet it is

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100

75 r s

e 68.3 w s n a

t 55.5 c 55 50 r e o c

f o %

25

0 2001 (300) 2006 (575) 2014 (165)

Year of study (sample size)

Figure 2 Trend in mean diabetes knowledge scores among patients in Al Ain city, United Arab Emirates

worth noting that the clinics we sur- of 165 participants (87.3%) indicated our study participants, as found else- veyed had diabetes educators, dieticians that glucose levels are best ascertained where (3). and educational materials, including by “how I feel”. This apparently wide- We observed weak associations locally developed patient handouts in spread misunderstanding leads patients with age (peaking at 41–50 years) and Arabic. The impact of these interven- to skip blood testing, while sustaining education as predictors of knowledge; tions on patient knowledge remains asymptomatic hyperglycaemia for ex- this, however, did not hold on multivari- unclear. tended periods. Diabetes educators in ate adjustment. In a recent study in the Comparing our mean score of 55% the region may need to emphasize the region, patients’ self-perceived knowl- correct responses with the results of “silent killer” role of diabetes, as well edge of diabetes declined with increas- other researchers who used the MDKT as the need for blood testing to assess ing age, supporting our findings 21( ). provides an interesting perspective. A glycaemic control. Al-Maskari and colleagues (3) reported study in Nigeria (14) reported a mean Misconceptions about diet are also several significant associations, possibly score of 44%, while a survey in the common. In our study, baked potatoes as a result of their larger sample size, United States of America (2) observed were not thought to be the highest in but with small differences. For instance, a mean score of 60%. Another study in carbohydrates, and low-fat milk was counselling by diabetes educators had the USA (20) involving older patients thought to be lower in fat than honey. minimal effect on patients’ knowledge found “poor” performance, with a score Notably, unsweetened fruit juice was and attitudes, and no effect on diet and of 64.9%. This last study reported cogni- believed by the majority of participants self-care. tive function and depression as inde- either to lower the blood glucose or There seems to be a tentative link pendent predictors of knowledge score. to have no effect – a fallacy that may between knowledge and outcomes: one The questions in the MDKT instru- stem from general recommendations study found that, for each increase in ment used in our study dealt with a fairly to eat more fruit or the notion that un- the number of questions answered cor- basic understanding of the diabetic diet. sweetened fruit juices have a low car- rectly on the MDKT, haemoglobin A1c For example, glucose levels are routinely bohydrate load. These misconceptions decreased by 0.239 (2). While intensive, measured using blood samples. Yet, may lead to persistent dietary patterns structured diabetes self-management when asked about the best method of that jeopardize diabetes management, education programmes increase knowl- assessing glucose levels, only 8.5% cor- despite optimal drug treatment. On edge and appear to improve glycaemic rectly chose blood samples, while 4.2% the other hand, knowledge of diabetes control, the effect is attenuated if the chose urine testing and, remarkably, 144 complications appeared satisfactory in baseline knowledge is already high (22).

746 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Thus, it may be preferable for diabetes a healthy lifestyle needs to start at an represent a considerable burden for education to be focused on patients early age in view of the high prevalence regional health systems. Additional ef- with low baseline knowledge. of obesity and metabolic syndrome forts are needed to improve diabetes Some authors have speculated that among adolescents in this region (27). education and long-term care. knowledge alone is not sufficient to Caution is needed in drawing infer- translate into the motivation needed ences from our study findings, because for improved self-care (23). Diabetes of the limited sample size, the restric- Ethical approval education efforts should incorporate tion of participants to Emirati Arabs behavioural strategies to motivate and only, and the lack of patient-oriented Research ethics approval was obtained enable patients to care for themselves outcomes. Nevertheless, our use of a prior to commencement of the study effectively. Even knowledge of diabetes validated instrument allows compari- from Al Ain Medical District Human goals, the “know your numbers” ap- sons with other locales as well as over Research Ethics committee, protocol proach, by itself does not lead to better time in the region. Taking into account number 09/38; CRD# 47/11. Addi- risk factor control (24). Thus, there ap- that our study was conducted at urban tionally, institutional approval was ob- pears to be a knowledge–practice gap university-affiliated clinics with tertiary tained from Tawam Hospital, Al Ain, to among patients with diabetes, which care support, the low levels of knowl- conduct research at its affiliated clinics. means that improving knowledge does edge are of concern and suggest that not lead to improved metabolic indica- conditions in rural settings may be even Acknowledgements tors (25). worse. Lack of knowledge may not be the We thank all study participants and limiting factor in these patients. Issues clinic nurses. We acknowledge the such as lack of motivation, absence of Conclusion Michigan Diabetes Research Center social support, competing demands, and paucity of culturally appropriate Knowledge of diabetes among patients (MDRC) as the source of the items in exercise settings for women may play a attending clinics in Al Ain city has the survey instrument. greater role (10). Social factors, such as remained low since 2001. With the Funding: The study was supported cultural practices and even economic marked rise in diabetes prevalence in by a generous grant from the Emirates limitations, affect patients with diabe- the UAE and neighbouring countries, Foundation. tes (26). Indeed, health promotion for this is a cause for concern as it could Competing interests: None declared.

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13. Fitzgerald JT, Funnell MM, Hess GE, Barr PA, Anderson RM, Hiss care services in the United Arab Emirates. Glob Health Promot. RG et al. The reliability and validity of a brief diabetes knowl- 2014;21:44–51. edge test. Diabetes Care. 1998;21(5):706–10. PMID:9589228. 22. Berikai P, Meyer PM, Kazlauskaite R, Savoy B, Kozik K, Fogelfeld 14. Jasper US, Ogundunmade BG, Opara MC, Akinrolie O, Pyiki L. Gain in patients’ knowledge of diabetes management targets EB, Umar A. Determinants of diabetes knowledge in a cohort is associated with better glycaemic control. Diabetes Care. of Nigerian diabetics. J Diabetes Metab Disord. 2014;13(1):39. 2007;30(6):1587–9. PMID:17372160. PMID:24593904. 23. Heisler M, Piette JD, Spencer M, Kieffer E, Vijan S. The relation- 15. Al-Qazaz HKh, Sulaiman SA, Hassali MA, Shafie AA, Sundram ship between knowledge of recent HbA1c values and diabetes S, Al-Nuri R et al. Diabetes knowledge, medication adherence care understanding and self-management. Diabetes Care. and glycemic control among patients with type 2 diabetes. Int J 2005;28(4):816–22. PMID:15793179. Clin Pharm. 2011;33(6):1028–35. PMID:22083724. 24. Stark Casagrande S, Ríos Burrows N, Geiss LS, Bainbridge KE, 16. Al-Adsani AMS, Moussa MA, Al-Jasem LI, Abdella NA, Al- Fradkin JE, Cowie CC. Diabetes knowledge and its relation- Hamad NM. The level and determinants of diabetes knowl- ship with achieving treatment recommendations in a na- edge in Kuwaiti adults with type 2 diabetes. Diabetes Metab. tional sample of people with type 2 diabetes. Diabetes Care. 2009;35(2):121–8. PMID:19250850. 2012;35(7):1556–65. PMID:22498806. 17. Michigan Diabetes Research Center. Diabetes knowledge 25. Bloomgarden ZT, Karmally W, Metzger MJ, Brothers M, Ne- test. Ann Arbor (http://diabetesresearch.med.umich.edu/ chemias C, Bookman J et al. Randomized, controlled trial of Tools_SurveyInstruments.php#dkt, accessed 11 October 2016). diabetic patient education: improved knowledge without 18. Rose M, Hildebrandt M, Fliege H, Seidlitz B, Cotta L, Schi- improved metabolic status. Diabetes Care. 1987;10(3):263–72. rop T et al. Relevance of the treatment facility for disease- PMID:3297575. related knowledge of diabetic patients. Diabetes Care. 26. Khatib M, Efrat S, Deeb D. Knowledge, beliefs, and economic 2000;23(11):1708–9. PMID:11092302. barriers to healthcare: a survey of diabetic patients in an 19. Hashim MJ, Prinsloo A, Mirza DM. Quality improvement tools Arab-Israeli town. J Ambul Care Manage. 2007;30(1):79–85. for chronic disease care–more effective processes are less PMID:17170641. likely to be implemented in developing countries. Int J Health 27. Mehairi AE, Khouri AA, Naqbi MM, Muhairi SJ, Maskari FA, Care Qual Assur. 2013;26(1):14–19. PMID:23534102. Nagelkerke N et al. Metabolic syndrome among Emirati ado- 20. Murata GH, Shah JH, Adam KD, Wendel CS, Bokhari SU, Solvas lescents: a school-based study. PLoS One. 2013;8(2):e56159. PA et al. Factors affecting diabetes knowledge in type 2 diabet- PMID:23418529. ic veterans. Diabetologia. 2003;46(8):1170–8. PMID:12856126. 21. Baynouna LM, Neglekerke NJD, Ali HE, ZeinAlDeen SM, Al Ameri TA. Audit of healthy lifestyle behaviors among patients with diabetes and hypertension attending ambulatory health

748 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Preliminary estimates of the economic implications of addiction in the United Arab Emirates C.M. Doran1

التقديرات األولية لآلثار االقتصادية لإلدمان يف اإلمارات العربية املتحدة كريستوفر دوران اخلالصــة: هدفــت هــذه الدراســة إىل تقديــم تقديــرات أوليــة لآلثــار االقتصاديــة لإلدمــان يف اإلمــارات العربيــة املتحــدة. وقــد اســتخدمت مصــادر بيانــات حمليــة ودوليــة الســتخالص تقديــرات لتكاليــف الرعايــة الصحيــة املرتبطــة بتعاطــي املــواد ولإلنتاجيــة املهــدرة بســبب تعاطيهــا وللســلوك اإلجرامــي الــذي ينجــم عــن ذلــك. فــكان مــن بــن الســكان الذيــن يقــدر عددهــم بـــ 8.26 مليــون نســمة: حــوايل 1.47 ًمليونــا يتعاطــون التبــغ )%20.5 مــن البالغــن(، و 380085يتعاطــون احلشــيش )<%5(، و14077 يتعاطــون الكحــول عــى نحــو ضــار )%0.2(، و1408 يتعاطــون املــواد األفيونيــة )%0.02(. وقــد قــدرت تكلفــة اإلدمــان بـــ 5.47مليــار دوالر أمريكــي يف عــام 2012، أي مــا يعــادل %1.4 مــن الناتــج 88 4.79 املحــي اإلمجــايل. وكانــت التكاليــف اإلنتاجيــة َ املســاهماألكــر حيــث بلغــت مليــار دوالر أمريكــي )% (، تالهــا الســلوك اإلجرامــي الــذي بلــغ 0.65 مليــار دوالر أمريكــي )% (. 12ومل تكــن هنــاك بيانــات لتقديــر تكلفــة كل مــن: معاجلــة األمــراض املرتبطــة بتعاطــي التبــغ، أو تثقيــف املجتمــع، أو جهــود الوقايــة، أو التنافــر االجتامعــي. إن اجلهــود املبذولــة ًحاليــا جلمــع البيانــات ذات قــدرة حمدودة عــى إعطــاء معلومات كافيــة للقيــام ٍّ بتصــدمناســب لإلدمــان يف اإلمــارات العربيــة املتحــدة. فهنــاك حاجــة إىل مــوارد لتحســن مــؤرشات تعاطــي املخــدرات ورصــد األرضار وتقييــم املعاجلــة.

ABSTRACT This study aimed to provide preliminary estimates of the economic implications of addiction in the United Arab Emirates (UAE). Local and international data sources were used to derive estimates of substance- related healthcare costs, lost productivity and criminal behaviour. From an estimated population of 8.26 million: ~1.47 million used tobacco (20.5% of adults); 380 085 used cannabis (> 5%); 14 077 used alcohol in a harmful manner (0.2%); and 1408 used opiates (0.02%). The cost of addiction was estimated at US$ 5.47 billion in 2012, equivalent to 1.4% of gross domestic product. Productivity costs were the largest contributor at US$ 4.79 billion (88%) followed by criminal behaviour at US$ 0.65 billion (12%). There were no data to estimate cost of: treating tobacco-related diseases, community education and prevention efforts, or social disharmony. Current data collection efforts are limited in their capacity to fully inform an appropriate response to addiction in the UAE. Resources are required to improve indicators of drug use, monitor harm and evaluate treatment.

Estimations provisoires des implications économiques des addictions aux Émirats arabes unis

RÉSUMÉ La présente étude avait pour objectif de fournir des estimations provisoires des implications économiques des addictions aux Émirats arabes unis. Des sources de données locales et internationales ont été utilisées pour produire des estimations sur le coût des soins de santé, la perte de productivité et les comportements criminels liés à la consommation de substances psychoactives. Sur une population estimée de 8,26 millions, 1,47 étaient consommateurs de tabac (20,5 % des adultes), 380 085 de cannabis (> 5 %), 14 077 consommaient de l’alcool de façon nocive (0,2 %), et 1408 des opiacés (0,02 %). Le coût des addictions a été estimé à 5,47 milliards de dollars US en 2012, soit 1,4 % du produit intérieur brut. Les coûts de productivité représentaient le facteur contributif le plus important (4,79 milliards de dollars US, soit 88 %), suivis par les comportements criminels (0,65 milliard de dollars US, soit 12 %). Aucune donnée n’était disponible pour estimer les coûts induits par le traitement des maladies dues au tabagisme, par l’éducation communautaire et les efforts de prévention, ou par les perturbations d'ordre social. Les efforts déployés actuellement pour collecter des données sont limités du fait de l’incapacité à mettre en place une réponse appropriée aux addictions aux Émirats arabes unis. Des ressources sont requises pour améliorer les indicateurs de la consommation de drogues, opérer un suivi des effets néfastes et déterminer le traitement.

1School of Human, Health and Social Sciences, Central Queensland University, Brisbane, Australia (Correspondence to: [email protected]). Received: 23/5/2015; accepted: 15/8/2016

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Introduction fertile environment for abuses such as NRC treatment costs illegal immigration, drug trafficking and The NRC is the only specialized ad- The use of addictive substances has a money laundering (5). Furthermore, diction centre in the UAE. The first wide variety of adverse health and social the economic and social changes seen phase of addiction treatment at NRC consequences (1). Substance use affects in the UAE since 1971 have catapulted is detoxification, which can take up to 2 the ability of individuals to function in a people from a nomadic and isolated life weeks; the second phase is short-term productive capacity; it has negative ef- into a luxurious lifestyle. To this extent recovery, which lasts for 8 weeks; and fects on education and employment; it many of the traditional values of the the halfway house phase, which takes reduces quality of life and makes people indigenous people have changed and up to 6 months. The outpatient clinic more susceptible to health problems; have been influenced by the values and follows up patients for 1 year after dis- it affects their self-esteem; and often attitudes of those who come to work in charge from the halfway house. forces them to engage in criminal be- the UAE. The rapid social change has A total of 933 patients were admit- haviour to support their addiction. At been an important factor behind the ted to the NRC treatment facility dur- the macro level, substance-related crime appearance of many types of antisocial ing 2002–2012, with 377 in 2012 (4). and corruption affect the Government’s behaviour, of which drug use is one. Services are provided to local people ability to address addiction-related The purpose of this study was to free of charge. Health statistics from harm effectively 2( ). provide preliminary estimates of the HAAD suggest an average inpatient Given the economic ramifications economic implications of addiction in cost of UAE Dirham (AED) 10 861 of substance use, policy makers are the UAE. (US$ 2957) with an average length of increasingly interested in understand- stay of 5.71 days, equivalent to AED ing the economic burden of addiction. 1902 (US$ 517.93) per day. The cost Methods Estimates of the economic costs of sub- per outpatient visit is AED 300 (US$ stance use serve many purposes. First, 81.69). At the NRC, an inpatient stay As outlined in the international economic cost estimates are frequently requires 3 months and an outpatient guidelines for estimating the costs of used to argue that policies on alcohol, visit is twice weekly for a further 9 addiction (3), the key types of costs as- tobacco and other drugs should be months. Combining this information sociated with substance abuse include: provides an estimate of NCR treatment given a high priority on the public policy consequences to the health system (i.e., agenda. Second, economic cost studies costs for local people [i.e., (US$ 517.93 treatment costs); productivity (i.e., pre- × 12 weeks × 7 days × 377 patients) + help to identify information gaps, re- mature mortality or lost employment search needs and desirable refinements (US$ 81.69 × 9 months × 2 visits per or productivity); law enforcement and week × 377 patients)]. to national statistical reporting systems. criminal justice; others (such as costs Third, improved estimates of the costs related to prevention and research); Health service cost of treating alcohol of substance abuse offer the potential and, intangible costs (i.e., social dishar- and substance abuse to provide baseline measures to deter- mony). Statistics on the number of admissions mine the efficacy of drug policies and for alcohol and substance abuse are programmes intended to reduce the Consequences to the health available from HAAD. In 2012, there damaging consequences of addictive system were 578 admissions with 486 (84%) substances (3). Healthcare provision in UAE originally referred from an outpatient The United Arab Emirates (UAE) The structure of health care in the UAE setting 4( , 6). With an estimated popu- has become a target for the international varies from one Emirate to another. lation in Abu Dhabi in 2010 of 2.32 illicit drug scene due to its strategic geo- In Abu Dhabi, there are 3 main bod- million (6), this equates to an admis- graphic location, openness, economic ies: the National Rehabilitation Center sion rate of 0.249 per 1000 population. prosperity and young population. (NRC), the Health Authority of Abu Combining this information with Drugs pass through the Middle East, in- Dhabi (HAAD) and the Abu Dhabi UAE population estimates (8.26 mil- cluding the UAE, from drug-producing Health Services Company. In , lion) (7), assuming the same rate of countries in South East Asia, Pakistan there are 2 main bodies: the Dubai service delivery and cost as reported in and Afghanistan on their way to meet- Health Authority and the Ministry of Abu Dhabi, an estimate can be made ing the high demand of users in drug- Health (MOH). The MOH is the regu- of hospital and outpatient alcohol and consuming countries in Europe and latory and provisional body for public substance abuse treatment costs for the North America (4). The open market and private healthcare facilities in Shar- entire UAE [i.e., (US$ 517.93 × 5.71 trade policy, a fundamental cornerstone jah, Ajman, Fujairah, Ras al-Khaimah, days × 2292 patients) + (US$ 81.69 × of the economy in the UAE, offers a Sharjah and Umm al-Quwain (4). 1926 patients)].

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Health service cost of treating tobac- bloodstream using needles. Sharing the UAE (i.e., 2292 inpatients and 1926 co-related diseases needles or using unhygienic needles outpatients); and multiplying with aver- Out of all substances, the evidence can lead to HIV infections and other age length of stay (i.e., 90 days as NRC relating to tobacco use is perhaps the blood-borne diseases (11). Given the inpatient, 5.71 days as hospital inpatient most advanced with associations be- lack of data on these possible side effects and 1 day per outpatient visit). or comorbidity in the UAE, no attempt tween tobacco use and a plethora of Opportunity cost of time while incar- was made to quantify these costs. diseases well-established (8). In 1994, cerated Lopez et al. suggested a 4-stage model Cost of substance-related lost When individuals are incarcerated they for describing the effects of tobacco productivity are often partially or totally removed smoking on mortality (9) illustrating Impact on quality and quantity of from the productive economy (3). This that smoking-attributed mortality is life constitutes a loss of potential productiv- seen several decades after smoking has As part of the Global Burden of Disease ity to the economy. This loss is deemed occurred. By depicting the epidemic (GBD) assessment, the Institute for to be justified on the basis of protecting as a continuum spread over many dec- Health Metrics and Evaluation provide other citizens and punishing offend- ades, the model allows countries to see disease estimates for the UAE (12). In ers, however, it does withdraw a certain themselves as being at a particular stage 2010 for the UAE, drug use, smoking number of people from the possibility of an understandable process, spread and alcohol use together accounted of participating in productive activities. over a whole century (9, 10). With the for almost 10% of the disease burden, While acknowledging this as a potential prevalence of smoking estimated at > equivalent to 140 548 DALYs. (or economic cost, this study did not at- 20% in the adult population (Table disability-adjusted life years). A value 1), the UAE is entering Stage 2 of this tempt to value the productivity costs of can be attached to a DALY by using incarcerated drug offenders. model. Given the lag effect between gross domestic product (GDP) per tobacco smoking and disease, deaths capita. GDP per capita in the UAE was Cost of drug-related criminal from tobacco will inevitably increase. At estimated at US$ 34 049 (13). behaviour the time of writing, there was no infor- In the UAE, law enforcement is the mation available on the treatment costs Opportunity cost of time while in treatment responsibility of each Emirate. Each associated with smoking, therefore no Emirate’s police force is responsible for estimate was attempted. While patients are in treatment they are not being productive members of matters within its own borders, but the Health service cost of treating prob- society. Productivity costs of treatment forces routinely share information with lems related to substance abuse can be estimated by: adjusting GDP per each other on various issues. The police As well as the direct cost of treating capita to a daily rate (US$ 34 049/48 in the UAE come under the Ministry alcohol and substance abuse, there are working weeks/5 working days); com- of Interior and are also responsible for costs associated with the treatment of bining with the number of admissions maintaining the prisons, and the arm side effects and comorbidity. For exam- to the NRC (i.e., 377 inpatients and responsible for this is the Corrections ple, certain users inject drugs into their 317 outpatients) and the hospitals in Department (14).

Table 1 Estimated prevalence of substance use in the UAE Type of substance Percentage of population Number of users Source (aged 15–64) Alcohol 0.2% 14 077 (19) Amphetamines No recent data No estimate (11) Cannabis 5.40% 380 085 (11) Cocaine No recent data No estimate (11) Ecstasy No recent data No estimate (19) Opioids 0.02% 1408 (11) Opiates 0.02% 1408 (11) Prescription opioids No recent data No estimate (11) Tobacco – youth (< 20 yr) 14.0% 80 248 (29) Tobacco – adults (20–64 yr) 20.50% 1 388 163 (29)

UAE = United Arab Emirates; WHO = World Health Organization.

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The main law regulating drug con- Incarceration costs Results trol in the UAE is the Anti-Drug and According to the prison affiliated focus Substance Use Law (41/4991). Drug group discussants in the NRC report Population estimates use and possession is considered an (4), prisoners believed that > 10% of the The UAE National Bureau of Statistics offence under this law and penalties total prison population were drug abus- estimated a population of 8.26 million vary according to the type of substance ers. Another data source suggests that people in 2010 (7). Non-nationals ac- (15). The legal process of drug-related the percentage of prisoners who are sen- counted for 89% (7.32 million) of the crimes and offences is organized in three tenced for substance abuse ranges from population and nationals for 11% (0.94 stages: police (arrested and charged 15 to 20% (4). Data from the United million). within 48 hours), general prosecution Nations Office on Drugs and Crime Prevalence of substance use (maximum 30 days) and then court. (UNODC) suggest that there may The punishments imposed on guilty have been 11 193 people incarcerated There are publically available local data persons in drug cases range from put- in the 14 adult prisons in the UAE 2008. on the prevalence of substance use in ting the person in a treatment centre, a Applying the same growth rate to the the UAE. These rely on data reported fine, imprisonment (temporary or life) number of incarcerated people as that in Drug Report (11, 18). or capital punishment. seen in the population between 2006 Table 1 provides an estimate of the number of substance users in the UAE. Cost of police resources devoted to and 2012 (i.e., 189%) (13) suggests Tobacco use was the most common combating drug problems that, in 2012, there could have been 21 substance used, with an estimated 1.47 A 2008 United Nations UAE country 113 prisoners. If 15% of this population million smokers (20.5% of adults); 380 report suggested that there were: 72 had been incarcerated for drug offences, 085 people (5.4% of the population) 670 recorded crimes; 971 reported this is equivalent to 3170 inmates. used cannabis and an estimated 14 077 drug offences (64 for trafficking); 3688 It is costly to employ prison staff and consumed alcohol in a harmful manner persons prosecuted; 125 prosecution operate a prison. In the absence of any (i.e., ≥ 60 g pure alcohol on at least one personnel; 14 adult prisons (with a better data, it is assumed that the daily occasion in the past 30 days) (19). To capacity of 6715); 3295 staff working cost of housing an inmate is equivalent date, there are no accurate estimates in the prisons; and, 11 193 people in- to the daily cost of an inpatient stay on the use, if any, of amphetamines, carcerated (16). It is reported that the (i.e., US$ 517.93) (6). Combining the cocaine, ecstasy, prescription opioids or Dubai Police Force has 15 000 officers. daily cost with the number of prison- injecting drugs (18, 20). Given that Dubai and Abu Dhabi are ers incarcerated for drug offences (i.e., the two largest Emirates, it may be as- 3170) suggests a daily cost of US$ 1.64 Preliminary estimates of the sumed that the size of the police force in economic cost of addiction in million. This cost can be extrapolated the UAE Abu Dhabi may be at least as big as that to an annual basis by multiplying with The economic cost of addiction in the of Dubai. Therefore, the police force in 365 days. the UAE is conservatively estimated to UAE is estimated at US$ 5.47 billion; be in excess of 30 000. Other costs of substance equivalent to 1.4% of GDP in 2012 (Ta- abuse ble 2). Substance-related lost productiv- At the time of writing, there were ity accounted for the majority of costs, no data on police resources devoted to There are several other costs to society 87.6% of the total or US$ 4.79 billion, combating drug problems in the UAE. of substance abuse, including: research followed by the cost of drug-related on the impact of substance use; public However, an Australian report found criminal behaviour at 11.9% of total education campaigns to minimize use that 5.9% of total police activity was costs or US$ 0.65 billion. spent on combating drug-specific activ- or abuse; law enforcement programmes ity (17). To derive an estimate of the to reduce illegal dealing and use; and police cost associated with combating the cost of social disharmony associated Discussion drug problems in the UAE, the number with substance abuse. Development of police devoted to combating drug of cost estimates for each of these cat- This study attempted to provide pre- problems (using a conservative esti- egories requires extensive data and such liminary estimates of the economic mate of 5% of police time) is multiplied information was not available at the implications of addiction in the UAE. with the average wage of a police officer time of writing, therefore, no estimates For those categories for which estimates (using GDP per capita of US$ 34 049). were attempted. were made, several assumptions were

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Table 2 Summary of estimated costs of addiction in the UAE Category US$ Notes Consequences to health and welfare system NRC treatment costs 16 956 175 Based on limited data from NRC Health service cost of treating alcohol and 6 937 071 Based on limited data from HAAD and substance abuse extrapolation to UAE Health service cost of treating tobacco- No estimate significant given the prevalence of related diseases tobacco use Health service cost of treating problems No estimate No available data related to substance abuse Cost of substance-related lost productivity Impact on quality of life and longevity 4 785 451 016 Places a dollar value on disability adjusted life years from global burden Opportunity cost of time while in treatment 6 988 807 Based on limited data from NRC, for substance abuse HAAD and extrapolated to UAE Opportunity cost of time while in treatment No estimate significant given the prevalence of for tobacco conditions tobacco use Opportunity cost of time while in treatment No estimate No available data for substance abuse related problems Opportunity cost of time while incarcerated No estimate No available data but likely to be for substance abuse offences significant Cost of substance-related criminal behaviour Cost of police force devoted to combating 51 072 776 Based on limited data – 5% of police drug problems force (assumed to be 30 000) devoted to drug control Cost of prosecution and operating courts No estimate No available data but likely to be significant Incarceration annual cost 599 274 078 Based on limited data – 15% inmates incarcerated for drug offenses, daily cost of US$ 517.93 Salary of prison staff No estimate No available data – partially included in daily cost of keeping inmates in gaol Other police costs in strategic alliances No estimate No available data but likely to be significant Other costs of substance use Cost of community education and No estimate No available data but likely to be prevention around substance abuse significant Education implications No estimate No estimate – likely to be significant given high drug use among youth Employment implications No estimate No estimate – likely to be significant as school drop-outs increase Social disharmony No estimate No estimate – likely to be significant as increase in crime and violence affects community sense of security Total cost substance use 5 466 679 923 GDP (2012) 383 799 194 081 % substance cost/GDP 1.4%

GDP = gross domestic product; HAAD = Health Authority of Abu Dhabi; NRC = National Rehabilitation Center; UAE = United Arab Emirates.

required. First, cost data obtained from was intensive, resulting in a high cost other Emirates compared with Abu HAAD were used to derive treatment for this particular specialist treatment Dhabi, derived healthcare costs would cost estimates. Treatment at the NRC setting. If costs were less expensive in be inflated. Conversely, there were no

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estimates of treating tobacco-related Lapsley estimated the social costs of treatment and harm reduction. Various diseases or other problems related to alcohol, tobacco and illicit drugs at US$ government agencies work closely with substance abuse, which suggests that 34.4 billion (23). Mark et al. estimated international entities like the United healthcare costs are generally conserva- the economic cost of heroin addiction Nations, Interpol and other countries tive. Second, most of the cost associated in the United States of America at US$ to stop the activities of drug traffickers. with lost productivity related to sub- 21.9 billion (24). García-Altés estimat- The government has also enacted laws stance abuse was derived by combining ed the social cost of the consumption that regulate drug control (4). the current global burden of disease of illegal drugs in Spain at US$ 0.467 estimates, using the DALY metric, billion (25). with estimates of economic output per Drug addiction is ubiquitous and a Conclusion capita. DALY estimates are subject to significant economic burden on UAE a high degree of uncertainty due to a society. Although the data may not be Governments are increasingly rely- lack of local data and the subsequent available at the moment to consider ing on evidence to inform policy. The need for statistical inferences about the the full spectrum of costs, the limited changes in drug use that are being re- UAE compared to other high-income information that is available points to ported in the UAE require a swift and countries (12). Furthermore, the as- a significant problem that may worsen sustained response. Such responses will sumption that the per capita income unless effective solutions are proposed be best developed using solid evidence of the whole population in the UAE is and implemented. In other developed that can be collected and disseminated applicable to non-locals might skew the countries, the ways in which govern- quickly to inform strategic policy re- estimates towards the higher end of the ments respond to drug addiction usu- sponses. Resources need to be devoted cost spectrum. Third, due to a lack of ally represent a blend of options across to improving the ability to identify, data, no estimates were made of costs different government portfolios, in- analyse and evaluate indicators of drug associated with efforts to educate the cluding policing and law enforcement, use, associated harm and treatment op- population to prevent the uptake of education, community and welfare tions. Current data collection efforts are substance abuse. services and health services. For exam- limited in their capacity to fully inform In spite of the methodological chal- ple, in Australia, one of the aims of the appropriate prevention, treatment and/ lenges, this analysis has demonstrated National Drug Strategy is “to achieve a or harm reduction responses. that substance abuse is a problem in the balance between harm-reduction, de- UAE with an estimated cost of addic- mand-reduction and supply-reduction tion placed at US$ 5.467 billion, equiva- measures to reduce the harmful effects Acknowledgements lent to 1.4% of total economic output. of drugs” (26). This approach has been This estimate is conservative given that echoed worldwide (11). The National The author would like to acknowledge not all costs were quantified. Drugs Policy in Switzerland emphasizes funding received from UNODC and Despite the apparent importance “the four pillar model as a pragmatic support provided by Dr Asma Fakhri. of costing studies, few researchers have middle way”, and aims to increase the Staff from the NRC assisted in iden- examined the economic impact of interchange between prevention, treat- tification of a range of local reports. addiction. Most efforts to date have ment, harm reduction and law enforce- Two anonymous reviewers provided considered costs associated with the ment (27). The latest American drug constructive comments on how to use and abuse of alcohol, tobacco and control strategy also emphasizes a bal- improve the quality of this manuscript. illicit drugs (21). Single et al. quantified ance between prevention, treatment, Any omissions or errors in analysis or the economic costs of alcohol, tobacco law enforcement and international interpretation of data rest solely with and illicit drugs to Canadian society at cooperation (28). In the UAE, the the author. US$ 18.4 billion, representing US$ 649 primary focus to date has been on de- Funding: None. per capita (22). In Australia, Collins and mand reduction with less attention on Competing interests: None declared.

References

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3. Single E, Collins D, Easton B, Harwood HJ, Lapsley H, Kopp drug%20policy%20expenditure%20in%20Australia%20-%20 P, et al. International guidelines for estimating the costs of 2009_10.pdf, accessed 29 September 2016). substance abuse. Geneva: World Health Organization; 2003. 18. World Drug Report 2011. Statistical annex: illicit drug consump- 4. Situation assessment of drug abuse in UAE: first phase second- tion. Vienna: United Nations Office on Drugs and Crime; 2012 ary data collection (2012–2013). Abu Dhabi: National Rehabili- (https://www.unodc.org/documents/data-and-analysis/ tation Center; 2014. WDR2011/StatAnnex-consumption.pdf, accessed 29 Septem- 5. Shihab M. Economic development in the UAE. In: Abed I, ber 2016). Hellyer P, editors. United Arab Emirates: a new perspective. 19. World Health Organisation. WHO Report on alcohol: United London: Trident Press; 2001: 249–59. Arab Emirates. Geneva: WHO; 2014 (http://www.who.int/ 6. Health Authority Abu Dhabi. Health statistics 2011. Abu Dha- substance_abuse/publications/global_alcohol_report/pro- bi: HAAD; 2012 (http://www.haad.ae/HAAD/LinkClick. files/are.pdf. Accessed 29 September 2016). aspx?fileticket=c-lGoRRszqc=, accessed 29 September 2016). 20. United Arab Emirates – Global AIDS response progress report 7. The World Bank. United Arab Emirates. http://data.world- 2012. Country progress report: United Arab Emirates; 2014 bank.org/country/united-arab-emirates, accessed 29 Sep- (http://files.unaids.org/en/dataanalysis/knowyourresponse/ tember 2016. countryprogressreports/2014countries/ARE_narrative_re- port_2014.pdf. Accessed 29 September 2016). 8. National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health. The health 21. Doran CM. Economic evaluation of interventions to treat opi- consequences of smoking – 50 years of progress: a report of ate dependence: a review of the evidence. Pharmacoeconom- the Surgeon General. Atlanta: Centers for Disease Control and ics. 2008;26(5):371–93. PMID:18429655 Prevention; 2014. 22. Single E, Robson L, Xie X, Rehm J. The economic costs of alco- 9. Lopez AD, Collishaw N, Piha T. A descriptive model of the hol, tobacco and illicit drugs in Canada, 1992. Addiction. 1998 cigarette epidemic in developed countries. Tob Control. 1994 Jul;93(7):991–1006. PMID:9744130 Sep;3(3):242–7. 23. Collins DJ, Lapsley HM. Counting the cost: estimates of the 10. Thun M, Peto R, Boreham J, Lopez AD. Stages of the ciga- social costs of drug abuse in Australia in 1998-9. National drug rette epidemic on entering its second century. Tob Control. strategy monograph series no. 49. Canberra: Commonwealth 2012;21(2):96–101. of Australia; 2002 (http://drogfokuszpont.hu/wp-content/ uploads/kokk_social_cost_australia_99.pdf, accessed 29 Sep- 11. United Nations Office on Drugs and Crime. World drug report tember 2016). 2014. 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Prevalence and seasonal variation of human intestinal parasites in patients attending hospital with abdominal symptoms in northern Jordan A.S. Jaran 1

انتشــار الطفيليــات املعويــة البرشيــة والتفــاوت املوســمي للعــدوىهبــا عنــد املــرىض الذيــن يراجعــون املستشــفى بأعــراض بطنيــةيف شــال األردن عدنان سليم جرن اخلالصــة: لقــد أجريــت هــذه الدراســة لتحديــد انتشــار الطفيليــات املعويــة والتفــاوت املوســمي للعــدوى هبــا يف شــال األردن. فقــد ُجعــت 3 5 2009 2013 4 21906 عينــات بــراز عــى مــدى ســنوات ) – ( مــن مستشــفيات حكوميــة يف مــدن. ُوجهــزت العينــات وفحصــت ًجمهريــا 41 44 9611 وبطــرق الرتكيــز. ُفعثــر عــى عــدوى طفيليــة يف عينــة )% (. كانــت اجليارديــة اللمبليــة أكثــر الطفيليــات ًانتشــارا )% (، تلتهــا املتحولــة احلالــة للنســج )% (31 واملتحولــة القولونيــة )%13(، وكانــت أقــل الطفيليــات ً انتشــاراالصفــر اخلراطينــي )%1(، واملحرشــفة القزمــة وأنــواع الرشيطيــات وشــفوية الســياط املنيليــة )جيعهــا >% (. 1وقــد اختلــف انتشــار الطفيليــات املختلفــة باختــاف املوســم، ففــي املتوســط أظهــرت أشــهر الصيــف أعــى حــدوث للعــدوى الطفيليــة )%62( مقارنــة مــع أشــهر الشــتاء )% (. 16وكانــت اجليارديــة اللمبليــة واملتحولــة احلالــة للنســج أكثــر ً انتشــارايف أشــهر الصيــف.

ABSTRACT This study was carried out to determine the prevalence of intestinal parasites and their seasonal variation in northern Jordan. A total of 21 906 stool samples were collected over a period of 4 years (2009– 2013) from 5 government hospitals in 3 cities. Samples were processed and examined microscopically and by concentration methods. Parasitic infection was found in 9611 samples (44%). Giardia lamblia was the most prevalent parasite (41%) followed by Entamoeba histolytica (31%) and Ent. coli (13%); the least prevalent parasites were Ascaris lumbricoides (1%), Hymenolepis nana, Taenia sp., and Chilomastix mesnili (all < 1%). The prevalence of different parasites varied according to season, on average the summer months showed the highest incidence of parasitic infection (62%) compared with the winter months (16%). Giardia lamblia and Ent. histolytica were most prevalent in the summer months.

Prévalence et variations saisonnières de parasites intestinaux humains chez des patients consultant en hôpital pour des symptômes abdominaux dans le nord de la Jordanie

RÉSUMÉ La présente étude a été menée afin de déterminer la prévalence de parasites intestinaux ainsi que leur variation saisonnière dans le nord de la Jordanie. Un total de 21 906 échantillons de selles ont été collectés sur une période de 4 ans (2009-2013) dans cinq hôpitaux gouvernementaux de trois villes. Les échantillons ont été traités et examinés à la microscopie et à l’aide de méthodes de concentration. Une infection parasitaire a été trouvée dans 9611 échantillons (44 %). Giardia lamblia était le parasite avec la prévalence la plus élevée (41 %), suivi par Entamoeba histolytica (31 %) et Entamoeba coli (13 %). Les parasites ayant la plus faible prévalence étaient Ascaris lumbricoides (1 %), Hymenolepis nana, Taenia sp., et Chilomastix mesnili (tous < 1 %). La prévalence des différents parasites variait en fonction de la saison : en moyenne, les mois d’été affichaient la plus haute incidence d’infections parasitaires (62 %) comparés aux mois d’hiver (16 %). Giardia lamblia et Ent. histolytica étaient les plus prévalents au cours des mois d’été.

1Department of Biological Sciences, Faculty of Science, Al-Bayt University, Mafraq, Jordan (Correspondence to: A.S. Jaran: [email protected]). Received: 15/07/15; accepted: 26/07/16

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Introduction Methods samples obtained from Princess Rahma Children's Hospital, Jerash and Ajlun Intestinal parasitic diseases are among Study design hospitals). the most common infections world- The study was conducted over a period wide and more prevalent in the poorest of 4 years (2009–2013) with the co- communities of the developing world operation of major hospitals in 3 cites. Sample collection (1–4). These infections are regarded as The fieldwork involved the collection and analysis a serious public health problem as they of stool samples from all patients at- Stool samples were collected in clean can cause iron-deficiency anaemia 5,6( ), tending these hospitals complaining of plastic containers and transferred to malnutrition (7), growth retardation in abdominal pain or stomach complaints. the microbiology laboratory at Al al- children and other physical and mental The study was carried out at hospi- Bayt University, where the experimental health disorders (8,9). Most clinicians tals in 3 main cities in northern Jordan, work was done. Patients were asked and health workers do not consider Irbid, Jerash and Ajlun, 3 hospitals in Irbid (Princess Badea, Princess Basma to provide fresh faecal samples. Stool parasitic infections as life threating, and and Princess Rahma Children's Hospi- specimens were examined for intestinal most of the time they go unnoticed or tal), 1 hospital in Jerash and 1 hospital parasites using the standard routine are misdiagnosed (10). Consequently, in Ajlun. These are all governmental methods used by hospitals and micro- not much attention is given to treating hospitals and serve a large population biological laboratories for diagnosing these diseases. of Jordanians, 1 626 300 in total (in- parasites (15). A direct saline smear Very few studies have been carried cluding 1 112 300 in Irbid, 187 500 in preparation was made and examined out in Jordan dealing with parasitic in- Jerash and 143 700 in Ajlun) accord- by light microscopy. For differential fections, and those that have been done ing to the latest census in 2015. North diagnosis of protozoa cysts, another only discussed specific cases or inci- Jordan is home to people living in di- preparation was made using Lugol's dents involving diarrhoea. Studies that verse socioeconomic conditions, from solution. Samples which did not show dealt with parasites either concentrated refugee camps (lower socioeconomic any intestinal parasites by direct smear on infants and children or adults in conditions) to modern cities with a high were examined using the zinc sulphate specific carriers such as food handlers standard of living. flotation concentration technique. For (11–14). The current study may be the The climate of north Jordan var- the detection of Enterobius vermicularis first comprehensive study to determine ies from very hot and dry during the cellophane tape preparation were used the prevalence of intestinal parasites summer months (June–September) to and examined either directly or by plac- over a long period in a large sample of cold and wet during the winter months ing 1–2 drops of xylene between tape (November–February). Stool samples Jordanians. and slide. Samples that were not exam- were obtained from patients attend- ined on the same day were kept at 4 °C. The aim of this study was to deter- ing the hospitals with stomach or ab- mine the prevalence of human intestinal dominal complaints (21 906 samples parasites and their seasonal variation in in total). The patients were divided into Statistical analysis the north of Jordan, where approximate- groups according to age, adults (> 15 ly a third of the Jordanian population years, samples obtained from Princess The chi-square test was used for com- live. Patients attending major hospitals Badea, Princess Basma, Jerash and Ajlun paring data. The level of significance was in Irbid, Jerash and Ajlun were studied. hospitals) and children (0–15 years, set at P < 0.05.

Table 1 Distribution of patients testing positive for intestinal parasite infection from hospitals in three cities in northern Jordan according to sex and age, 2009–2013 City Sex (P = 0.673) Age (years) (P = 0.04) Male Female 0–15 >15 Total No. % No. % No. % No. % Irbid 1614 51 1551 49 1070 33.8 2095 66.2 3165 Jerash 2391 48.1 2576 51.9 902 18.8 3890 81.2 4967 Ajlun 724 49 755 51 515 34.8 964 65.2 1479 Total 4729 50.3 4882 49.7 2487 26.4 6949 73.6 9611

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Table 2 Distribution of intestinal parasite species in three main cities in northern Jordan, 2009–2013 Parasite Irbid Jerash* Ajlun* Total Giardia lamblia 1234 2405 314 3953 Entamoeba histolytica 1312 1325 384 3021 Entamoeba coli 420 562 272 1254 Enterobius vermicularis 115 292 227 634 Trichomonas hominis (vaginalis) 140 240 153 533 Hymenolepis nana 17 38 37 82 Taenia sp. 12 27 9 48 Ascaris lumbricoides 24 42 18 84 Chilomastix mesnili 2 – – 2

*P < 0.05.

Results prevalence of parasitic infection than prevalent in the summer months (Ta- those from Ajlun (P < 0.05) (Table 2). ble 3). A total of 21 906 stool samples were col- Giardia lamblia was the most preva- lected over the study period of 4 years, lent parasite (41%), followed by Ent. Discussion of which 9611 samples tested positive histolytica (31%) and Ent. coli (Table 3). for parasitic infection (44%). The sex The prevalence of different parasites Parasitic infections occur most com- and age distribution of patients that varied in different seasons: on average monly in poor areas with low standards showed positive results are shown in of hygiene. In Jordan, parasitic infection Table 1. Sex of the patient did not show the summer months (June–Septem- ber) showed the highest incidence of has been found to be most prevalent in any statistical significance in relation rural areas and refugee camps (16). The parasitic infection (62%), with a peak in to the presence of intestinal parasites, current study shows that intestinal para- (P = 0.673); however, the relationship September, compared with the winter sitic infections are common in urban with age was statistically significant P( months (November–February) (16%), areas of Jordan (44%), with Giardia lam- = 0.043). with a peak in January; this was statis- blia the most prevalent parasite (41%), Patients attending hospital in Irbid tically significant P( < 0.05). Giardia followed by Ent. histolytica (31%). This and Jerash had significantly higher lamblia and Ent. histolytica were the most is in agreement with a 2007 study by

Table 3 Seasonal distribution of intestinal parasites in stool specimens in three main cities of northern Jordan, 2009–2013 Month No.of No. (%) No. (%) of parasite species identified in infected stool samples specimens infected examined GL EH EC TH EV Ts HN CM AL January 1056 103 (10) 25 (24) 34 (33) 32 (31) 12 (12) – – – – – February 2023 238 (12) 95 (40) 77 (33) 63 (27) – – – 3 – – March 1875 598 (32) 236 (39) 214 (36) 69 (12) 25 (4) 32 (5) 5 (1) 8 (1.4) – 9 (1.6) April 1798 999 (56) 482 (48) 238 (24) 216 (22) – 30 (3) 7 (<1) 11 (1) – 15(1.5) May 2594 1194 (46) 540 (45) 404 (33) 108 (9) – 112 (9) 8(<1) 9 (<1) – 13 (1) June 2592 1412 (54) 632 (45) 414 (29) 127 (9) 105 (7) 105 (7) 6 (<1) 12(<1) – 11 (<1) July 2620 1397 (55) 591 (42) 526 (38) 94 (7) 75 (5) 81 (6) 8 (<1) 12(<1) – 10 (<1) August 2356 1299 (55) 602 (46) 463 (36) 117 (9) 43 (3) 38 (3) 7 (<1) 13(1) 2 (< 1) 14 (1) September 1234 1032 (84) 315(30) 267 (26) 208 (20) 126 (12) 96 (9) – 8(<1) – 12(1) October 1345 836 (62) 235 (28) 203(24) 107 (13) 140 (17) 138 (16) 7 (< 1) 6 (<1) – – November 1379 294 (21) 115 (39) 103 (35) 76 (26) – – – – – – December 1034 209 (20) 85 (41) 78 (37) 37 (18) 7 (3) 2 (1) – – – – Total 21906 9611(44) 3953 (41) 3021 (31) 1254 (13) 533 (6) 634 (7) 48 (< 1) 82 (< 1) 2 (< 1) 84 (1)

GL = Giardia lamblia; EH = Entamoeba histolytica; EC = Entamoeba coli; TH = Trichomonas hominis (vaginalis); EV = Enterobius vermicularis; Ts = Taenia sp.; HN = Hymenolepis nana; CM = Chilomastix mesnili; AL = Ascaris lumbricoides.

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Chazal and Adi (14), who reported that histolytica (9.7%) followed by Giardia be paid to the problem. Treating these Ent. histolytica was the most frequent lamblia (4.1%) (19). The difference infections is of the utmost importance intestinal parasites followed by Giardia between our results and theirs may be along with prevention by giving advice lamblia. They also reported low inci- a reflection of the difference in sample to patients on hygiene and general dence of Ascaris lumbricoides, Enterobius size and duration of the study. Com- cleanliness. Attention should be focused vermicularis, Strongyloides stercoralis and paring our results to other studies in on public health education. Turkey, which has colder winters and Trichomonas hominis. They also noted Our research had shed light on higher incidence of infections with milder summers, the most prevalent the prevalence of parasitic infection in Ent. histolytica in spring and summer intestinal parasite was Enterobius ver- northern Jordan; for a better under- months compared with autumn and micularis (13.8%) followed by Giardia standing of the problem in Jordan as winter, which is also in agreement with intestinalis (6.1%) and Ent. coli (4.6%) a whole, and for more reliable data to the findings of the current study. In (20,21). In general Giardia lamblia and another study done in Jordan in 2006, Ent. histolytica were found to be the most consolidate the results, a further survey Giardia lamblia (61.5%) and Ent. histo- prevalent intestinal parasites compared is needed, which should involve most of lytica (19.6%) were the most prevalent with helminth infestation. the hospitals and clinics in the country. intestinal parasites in the Amman area Some clinicians and public health (central Jordan) (17). In Saudi Arabia workers do not consider intestinal Acknowledgements a 2011 study showed that the majority parasites to be an important problem of patients were infected by Ent. histol- so infected people are commonly not We are grateful to the staff of all primary ytica (4.7%) and Giardia lamblia (1.3%) treated or improperly treated, especially health care centres and all patients in- (18); Ancylostoma duodenale exhibited for worm infections (21). Our findings cluded in this study for their support the lowest prevalence. A study carried should change the view of most clini- out at Al-Najah University in the West cian in Jordan: intestinal parasitic infec- and assistance. Bank in 2011 also found that the most tions are important issues facing the Funding: None. prevalent intestinal parasite was Ent. population and more attention should Conflict of interests:None declared.

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18. Zaglool DAM, Khodari YAW, Gazzaz ZJ, Dhafar KO, Shaker 20. Okyay P, Ertug S, Gultekin B, Onen O, Beser E. Intestinal para- HAS, Farooq MU. Prevalence of intestinal parasites among sites prevalence and related factors in school children, a west- patients of Al-Noor Specialist Hospital, Makkah, Saudi Arabia. ern city sample–Turkey. BMC Public Health. 2004 Dec;4:64. Oman Med J. 2011 May;26(3):182–5. PMID:22043412 PMID:15615592 19. Hussein AS. Prevalence of intestinal parasites among school 21. Aksoy U, Akisü C, Bayram-Delibaş S, Ozkoç S, Sahin S, Usluca children in northern districts of West Bank-Palestine. Trop Med S. Demographic status and prevalence of intestinal parasitic in- Int Health. 2011 Feb;16(2):240–4. PMID:21073639 fections in schoolchildren in Izmir, Turkey. Turk J Pediatr. 2007 Jul–Sep;49(3):278–82. PMID:17990581

760 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Report Overview of the 63rd session of the WHO Regional Committee for the Eastern Mediterranean Ala Alwan 1

The 63rd session of the Regional more planned up to April 2017. The urged the necessity for cooperation Committee for the Eastern Mediter- Regional Committee was also invited between Member States to develop an ranean was held at the WHO Regional to provide comments on the WHO evidence-based integrated policy to im- Office in Cairo, Egypt, 3–6 October draft global implementation plan for prove access to assistive technology for 2016, attended by representatives of the recommendations of the Review all as an essential component of health the 22 Members of the Committee, Committee on the Role of the IHR service delivery systems, supported by along with observers from other UN in the Ebola Outbreak and Response. adequate financing, and to conduct a and intergovernmental organizations As part of its conclusion, the Regional needs assessment using appropriate and nongovernmental organizations. Committee highlighted the importance WHO tools to inform adequate plan- The achievements, challenges and of compliance with the regulations and ning of services. way forward for WHO in the Region maintaining core capacities, along with Public health deliverance and pro- formed much of the agenda, given that the key role of multisectoral coordina- motion of universal health coverage the overarching goal of WHO’s work tion in this, and the need to focus on clearly requires the support of effective with Member States since 2012 focused mass gatherings. and adequate blood transfusion and upon the five strategic priorities, namely: Improving access to assistive tech- health laboratory systems. The Regional health systems strengthening towards nology is an area that needs addressing Committee discussed the proposed universal health coverage; maternal in light of the protracted crises in the strategic frameworks which aimed at and child health; noncommunicable Region and resulting numbers of people enabling countries to ensure that their diseases; health security and com- with disabilities. The Regional Commit- national laboratory systems were well- municable diseases; and emergency tee discussed the need to increase ac- coordinated, sustainable, accessible for preparedness and response. The Re- cess to assistive technology and ensure all and able to generate safe, reliable and gional Director’s Annual Report, which its integration in universal health cover- timely results for public health purposes was presented and discussed during age, and suggested the need to redefine and patient care. In addition, discus- the Regional Committee, emphasized assistive technology on a broader basis sions covered the development and the main achievements with respect and to change the way assistive products strengthening of their national blood to these strategic priorities for WHO’s are designed, distributed and financed. systems to ensure the continuity, suf- work in the Region. This point was emphasized by several ficiency, sustainability and security of An update on the implementation representatives present who drew at- national supplies of safe and efficacious of the International Health Regula- tention to multisectoral collaboration blood and blood components to meet tions (IHR 2005) was brought to the as critical for the identification of needs national needs. The need to integrate attention of the Regional Committee and the provision of assistive products, laboratory and blood transfusion servic- through the work of the independent as well as the role of primary health care es within vertical health programmes, regional assessment commission, es- in needs identification, provision and and support in quality assurance and tablished in accordance with resolution follow-up of utilization. Moreover, at- laboratory accreditation were highlight- EM/RC62/R.3 to assess and advise tention was drawn to the importance ed, and not excluding the importance Member States. It made a number of a legal framework for the adoption of strengthening the public health and of recommendations to countries to of policies and programmes related to epidemic preparedness roles of health accelerate IHR implementation in assistive technology, and for capacity- laboratory services. The proposed stra- the Region, following joint external building and mechanisms to provide tegic frameworks were endorsed by evaluation assessments conducted in assistive products at affordable cost. the Regional Committee, which asked six countries in the Region, with nine To this end, the Regional Committee Member States to develop national

1 Regional Director, WHO Regional office for the Eastern Mediterranean, Cairo, Egypt

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plans accordingly and requested WHO Thus, Member States were encouraged supported WHO in providing further to provide support in this regard. to incorporate the family practice ap- technical guidance in the Region for Advancing family practice towards proach into their primary health care assessment of emergency care services; universal health coverage in the Re- services as an overarching strategy to organizing an intercountry consulta- gion received notable attention by advance towards universal health cover- tive meeting on genetic and congenital the Regional Committee, which dis- age. In addition, strengthening the ca- disorders; and submitting an evidence- cussed the need for comprehensive pacity of family medicine departments based plan of action for the regional and sustainable national policies and in public health facilities and medical implementation of the global roadmap programmes on family practice, to- education institutions was highlighted to address the health impacts of indoor gether with a framework for action for in order to increase the number of fam- and outdoor air pollution to the 64th Member States and WHO. However, ily physicians and to establish bridging session of the Regional Committee. representatives highlighted some of the programmes for general physicians. We thank representatives from the constraints to scaling up family practice WHO’s work in the Region has had 22 Members of the Regional Commit- in the Region and stressed the need for an important and effective impact, sup- tee and observers for their contribu- reform of medical education curricula, porting the needs and rights of citizens tions to the work WHO undertakes an operational guide linking family to universal health coverage in what in the Region with dedication, and the practice with secondary care, and stand- continues to be very difficult times due Committee’s recognition of the valu- ardization of bridging programmes as a to ongoing regional conflicts exacerbat- able developments and initiatives that transitional arrangement to upgrading ing health services degradation. Look- WHO has brought to fruition in the general physicians to family physicians. ing forward, the Regional Committee Eastern Mediterranean Region.

762 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Review Dietary transition and obesity in selected Arabic- speaking countries: a review of the current evidence B.H. Aboul-Enein 1, J. Bernstein 2 and A.C. Neary 3

التحول الغذائي والسمنة يف بلدان منتقاة ناطقة باللغة العربية: استعراض لألدلة احلالية باسل أبو العينني، جرشو برينشتاين، أنجيال نريي اخلالصــة: لقــد أصبــح تصاعــد معــدالت الســمنة إحــدى مشــاكل الصحــة العامــة الكبــ ة رييف إقليــم الــرق األوســط وشــال أفريقيــا، وكان ذلــك ًمرتبطــا بالتحــوالت نحــو نظــام غذائــي غــريب. ولقــد هــدف هــذا االســتعراض التكامــي إىل دراســة االجتاهــات والتحــوالت الغذائيــة احلاليــة وارتباطهــا بالســمنة يف البلــدان الناطقــة بالعربيــة يف إقليــمالــرق األوســط وشــال إفريقيــا. فجــرى البحــث يف قواعــد البيانــات ذات الصلــة عــا أجــري مــن دراســات يف بلــدان هــذا اإلقليــم بــني عامــي 1998 و2014 الســتقصاء اجتاهــات الســمنة والتغــريات التــي حدثــت يف أنــاط النظــم الغذائيــة عــى املســتوى اإلقليمــي لــدى مجيــع الفئــات العمريــة. فكانــت هنــاك 39 مقالــة تفــي بمعايــ رياالشــت ل. موقــد أشــارتمجيــع املقــاالت إىل حــدوث انتشــار للســمنة عــى نحــو متزايــد، وابتعــاد عــن األنــاط الغذائيــة التقليديــة، فذكــرت %51 منهــاحــدوث حتــول نحــو نظــام غذائــي غريب، – ووجــدت نصفهــا أن النظــام الغذائــي الغــريب قــد ارتبــط بزيــادة الســمنة. لقــد بــات مــن َّاملــرر - ًثقافيــا وضــع اســراتيجيات معنيــة بالتثقيــف الصحــي الغذائــي وبتعزيــز الصحــة ملواجهــة ٍّكل مــن التحــوالت الغذائيــة نحــو النظــام الغذائــي الغــريب والســمنة املتزايــدة.

ABSTRACT Escalating obesity rates have become a significant public health problem in the Middle East and North Africa (MENA) region and have been associated with shifts towards a westernized diet. This integrative review aimed to examine the current dietary trends and transitions and their association with obesity in Arabic-speaking countries of the MENA region. Relevant databases were searched for studies in MENA countries between 1998 and 2014 that investigated obesity trends and changes in dietary patterns at the regional level in all age groups. A total of 39 articles fulfilled the inclusion criteria. All the articles noted that obesity was increasingly prevalent and that there was a significant dietary shift away from traditional dietary patterns; 51% reported a shift towards a westernized diet and half found that the western diet was correlated with increased obesity. Culturally relevant dietary health education and health promotion strategies are warranted to address both the dietary shifts towards the westernized diet and the increasing obesity.

Transition alimentaire et obésité dans une sélection de pays arabophones : examen des données actuelles

RÉSUMÉ L’augmentation rapide des taux d’obésité est devenue un problème de santé publique significatif dans la région du Moyen-Orient et de l’Afrique du Nord (MENA) et est associée à une occidentalisation des habitudes alimentaires. Le présent examen intégratif visait à étudier les tendances et les transitions alimentaires actuelles ainsi que leurs associations à l’obésité dans des pays arabophones de la région MENA. Des recherches ont été menées dans des bases de données pertinentes afin de trouver des études réalisées dans les pays de la région MENA entre 1998 et 2014 portant sur les tendances de l’obésité et les changements d’habitudes alimentaires parmi tous les groupes d’âge au niveau régional. Au total, 39 articles répondaient au critère d’inclusion. Tous les articles mentionnaient que l’obésité était de plus en plus prévalente et qu’un éloignement notable des habitudes alimentaires traditionnelles s’opérait. En effet, 51 % des articles rapportaient une occidentalisation de l’alimentation, et la moitié concluait qu’il y avait une corrélation entre l’alimentation occidentale et l’augmentation de l’obésité. Une éducation en santé alimentaire et des stratégies de promotion de la santé pertinentes d’un point de vue culturel sont requises pour s’attaquer à la question de l’occidentalisation des habitudes alimentaires et de l’augmentation de l’obésité.

1School of Health Sciences, University of South Dakota, Vermillion, South Dakota, United States of America (Correspondence to: B.H. Aboul- Enein: [email protected]; [email protected]). 2College of Graduate Health Studies, A.T. Still University of Health Sciences, Kirksville, Missouri, United States of America. 3Kinesiology, Health Science, and Athletics, Cuesta College, San Luis Obispo, California, United States of America. Received: 07/07/15; accepted: 03/08/16

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Introduction transitions, particularly in developing Methods countries (8,9). The Westernized diet Global obesity is a wide-reaching has been identified as the leading dietary An integrative review of the literature epidemic that continues to create component contributing to this overall was carried out using a combination public health challenges, particularly in global nutrition transition (6). It has of the following search terms: obesity; developing countries (1). More than been characterized as a simultaneous diet; nutrition; transition; trend; shift 1.9 billion adults, 18 years and older, increase in the consumption of refined and Algeria; Bahrain; Egypt; Iraq; are estimated to be overweight (body sugars, animal fat, salt and red meats, Jordan; Kuwait; ; Libya; mass index [BMI] 25-29.9 kg/m2), and a decrease in the consumption of Mauritania; Morocco; Oman; Qatar; representing 39% of the world adult dietary fibre, fruits, vegetables, unrefined Saudi Arabia; Sudan; Syria; Tunisia; population (38% of men and 40% of whole grains and unsaturated fatty acids United Arab Emirates; Yemen; Pales- women). Of these overweight adults, which predisposes populations of devel- tinian Territories. Articles pertaining to over 600 million are obese (BMI 30- oped countries to chronic diseases (10). the general populations were selected. 39.9 kg/m2). These are the 2014 figures While there have been dietary Nine academic electronic databases from the World Health Organization transitions across developing countries (WHO) and are the most recent global including in the MENA region, with an were searched: PubMed, Scopus, data available (2). unfavourable dietary trend towards a ProQuest, EBSCOhost, SpringerLink, In countries of the Middle East and Westernized diet (9,11,12), there have ArticleFirst, Taylor & Francis, Wiley North Africa (MENA), the prevalence been insufficient attempts to provide Online, and ScienceDirect. Academic of obesity has significantly increased an integrative review of the published databases were selected because of their over the last 3 decades (3) with subse- literature on the current dietary trends academic rigor, aim, biomedical scope quent increases in obesity-related co- and transitions and their association and accessibility. At the same time, morbidities, including cardiovascular with the prevalence of obesity in the references from retrieved articles were diseases, chronic respiratory diseases, MENA region. At the same time, there reviewed to identify additional relevant diabetes, hypertension, metabolic syn- has been notable growth in the number publications. drome and some types of cancer (1,3). of studies on the growing obesity crisis According to the WHO 2014 fig- facing the MENA region. Addressing Inclusion/exclusion criteria ures, the Eastern Mediterranean Re- dietary trends to help reduce obesity The search was limited to articles gion has the third highest mean BMI and obesity-related mortality and mor- published between January 1998 and after North America and Europe (4). bidity is currently an important topic The highest levels of overweight and January 2015 and English language on the world health agenda (6,13) and obesity are found in Egypt, Bahrain, publications. Inclusion criteria for po- a crucial factor in establishing public Jordan, Kuwait, Saudi Arabia and the tential articles included cross-sectional health nutrition priorities and interven- United Arab Emirates for adolescents studies, literature reviews, meta-analysis, and adults aged 15 years and older; the tions. Therefore the purpose of this policy reports, analysis, or position paper was to identify the present dietary prevalence of overweight and obesity in statements. To be considered a poten- trends and transitions associated with these countries ranges from 74% to 86% tial article that provided evidence to obesity in Arabic-speaking countries in women and 69% to 77% in men (5). address this review, the article’s aim and through an integrative review of the The nutrition transition model, ini- scope had to address the relationship literature. Such a review could lead to tially proposed by Popkin in 1993, has between diet, transition and obesity been defined as a rapid global change a better understanding of the current status of obesity research in this region within the specified search parameters in food intake, sedentarianism, and stated above. Non-peer reviewed publi- their effects and health outcomes on and the type of future research needed. cations, dissertations and grey literature diet-related diseases (6). The foremost For the purposes of this study, Ar- were excluded from this review. Articles health outcome of the nutrition transi- abic-speaking countries of the MENA tion is the increased prevalence of global region were included, namely: Algeria, were categorized by study design, age obesity (7). The nutrition transition has Bahrain, Egypt, Iraq, Jordan, Kuwait, group, article focus (nutrition, obesity, been marked by a dietary shift in both Lebanon, Libya, Mauritania, Morocco, or both), dietary shift findings, correla- consumption and energy expenditure Oman, Qatar, Saudi Arabia, Sudan, Syr- tional findings and geographic location; as it relates to changes in demographic, ian Arab Republic, Tunisia, United Arab all age group categories were reported epidemiological and socioeconomic Emirates, Yemen and Palestine. using the publication authors’ criteria.

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Results 2). Among 12 articles that included (19). A cross-sectional survey (20) in children and adults, 5 reported obesity Morocco indicated that adherence to a The search processes identified 26 728 and 4 reported a Westernized diet shift; Mediterranean diet has decreased with citations. After abstract and full text 2 found a correlation between obesity dietary patterns transitioning towards screening, 39 studies were considered and Westernized diet (Table 2). All 19 a Westernized diet pattern. Another relevant and were included in the re- publications that noted both a dietary cross-sectional study in Kuwait in- view (Table 1). Table 1 summarizes shift and a Westernized diet shift found dicated that the Kuwaiti population the characteristics and results of the a positive correlation between the two. was experiencing a dietary transition, 39 studies. Twenty-eight of the articles evidenced by a high consumption of were published within the last 10 years. calorically dense foods that are low in Twenty-four focused on obesity, 13 on Discussion total dietary fibre and micronutrient nutrition and 2 on both. Eleven papers density (21). Recent studies indicate included children 18 years and younger, A large majority of articles focused on that consumption of fruits and vegeta- 16 included adults 18 years and older obesity as a static condition and not a bles among the Saudi population con- and 12 included data from all popula- causation or result. While 13 articles tinues to fall below the WHO dietary tion groups age 5 years and older. Fur- mentioned nutrition as a significant recommendations (22,23). Within the ther reduction and stratification of age contributor, most focused on obesity as context of these results there was a con- groups using individual author defini- the primary issue. To describe incidence sistent relationship between a Western- tions would have produced categories and prevalence of obesity in place of nu- ized diet and overweight and obesity. too small and inconsistent for statisti- tritional trends with strong correlations These studies continue to support an cally significant analyses. The sample to obesity is somewhat out of date. As a urgent need to increase culturally con- included 21 cross-sectional studies, 6 result, our study could not assess nutri- gruent nutrition awareness for healthy literature reviews, 6 reports, 5 analysis tion as preventive or protective factors food choices. Additionally, age also pre- papers and 1 position statement. for overweight and obesity. Nutritional sented as a potentially significant factor All articles noted a significant shift content represents a single element for tailored nutrition interventions and away from traditional dietary practices within a dietary shift; preparation and further research. for their respective regions and coun- cooking methods, caloric intake, meal The current trends in the United tries. Nineteen of the studies observed frequency, and portion size are variables States reveal how the Westernized diet a dietary shift away from a traditional not specifically or individually consid- contributes to incidence and prevalence diet and towards a Westernized diet, ered when discussing dietary shift. rates for overweight and obesity. Future while, 20 showed a dietary shift away Some recent articles highlight the research into dietary shifts in the MENA from traditional dietary practice but not current alarming levels of obesity and region associated with overweight towards a Westernized diet. predictions for obesity in Arabic-speak- and obesity could include predictive In 25 studies there were correlations ing countries (14–16) and continue analysis that incorporates similar vari- between obesity and poor nutrition, in to indicate an unfavourable dietary ables from developed countries where 16 there was decreased physical activ- trend towards a Westernized diet in the Westernized diet is prevalent (e.g. ity, 14 compared urban versus rural set- the MENA (17,18). The Westernized United States, Northern Europe). ting and 8 reported anecdotal findings diet was identified as a significant con- The articles included covered pub- such as cultural norms and snacking tributor to obesity in half of the articles lications from 1998 to 2014 but the or additional meals. Age presented as a included. In articles that identified a majority of articles were published in significant correlational finding in terms general dietary shift, correlations were the last 10 years which may signify an of obesity and a shift to a Westernized noted between a Westernized diet and increase in research on obesity in the diet. Nine of 11 articles investigating incidence and prevalence of obesity in MENA region. A historical review of the children reported obesity and 7 found the MENA region. The link between literature that predates electronic jour- a positive shift towards a Westernized shifts from traditional regional dietary nals would likely reveal other relevant diet; 5 of these studies reported positive patterns towards a Westernized diet is articles and could provide more his- a correlation between obesity and a remarkable within this sample of peer- torical insight into the trends in obesity Westernized diet (Table 2). Twelve of reviewed articles. For example, Leba- and diet. Understanding the potential the 16 articles on adults included obe- non has experienced a transition from effects of a westernized diet with regard sity with 8 reporting a Westernized diet a typically Mediterranean style of diet to overweight and obesity and utilizing shift; 5 showed a correlation between towards convenience foods, particularly the online publishing on investigational obesity and a Westernized diet (Table among young adults and adolescents studies in the MENA region could

765 EMHJ • Vol. 22 No. 10 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

Table 1 Summary of literature search Study (Year) (reference) Study design Age groupa Nutrition Western diet Region/Country/Territory (years) (N) or (Yes/No) Obesity (O) or Both (B) Kilpi et al. (2014) (15) Literature 15+ O Y Bahrain, Egypt, Iran, Jordan, Kuwait, review Lebanon, Oman, Saudi Arabia, Turkey Tayyem et al. (2014) (34) Cross-sectional 14-18 O Y Jordan Ng et al. (2014) (35) Literature Children & O N MENA region review adults Al Nohair (2014) (16) Report 18+ O Y Bahrain, Kuwait, Qatar, Oman, Saudi Arabia, Lebanon, UAE Regaieg et al. (2014) (36) Cross-sectional 9-12 O N Tunisia Musaiger et al. (2014) (37) Cross-sectional 15-18 O Y Bahrain Al-Quwaidhi et al. (2014) Analysis 25-64 O Y Saudi Arabia (38) Zaghloul et al. (2013) (21) Cross-sectional Children & N Y Kuwait adults Boutayeb et al. (2013) (39) Literature 18+ O N Eastern Mediterranean Region review Musaiger et al. (2013) (17) Cross-sectional 15-18 N Y Algeria, Jordan, Kuwait, Libya, Palestine, Syrian Arab Republic, UAE Musaiger et al. (2013) (40) Cross-sectional 5-18 O N Kuwait, Libya, Palestine, Syrian Arab Republic, UAE El Rhazi et al. (2012) (20) Cross-sectional 18+ N Y Morocco Ramdani et al. (2012) (41) Cross-sectional 40+ O N Morocco Golzarand et al. (2012) (11) Analysis Children & N Y MENA region adults Elmehdawi & Albarsha Report 18+ O Y Libya (2012) (42) Nagwa et al. (2011) (43) Cross-sectional 10-18 O Y Sudan Ng et al. (2011) (44) Cross-sectional Children & N N UAE adults Badran & Laher (2011) (14) Report 5-18 O Y MENA region Musaiger (2011) (45) Literature Children & O Y Eastern Mediterranean Region review adults Al-Hazzaa et al. (2011) (18) Cross-sectional 14-19 N Y Saudi Arabia Saker et al. (2011) (46) Cross-sectional 6-8 O N Algeria Musaiger et al. (2011) (47) Position Children & O Y MENA region Statement adults Musaiger et al. (2011) (48) Literature Children & N N MENA region review adults Ng et al. (2011) (49) Literature Children & O N Bahrain, Kuwait, Qatar, Oman, Saudi review adults Arabia, UAE Yahia et al. (2008) (19) Cross-sectional 18-24 B Y Lebanon Zindah et al. (2008) (50) Cross-sectional 18+ O N Jordan Fouad et al. (2006) (51) Cross-sectional 18+ O N Syrian Arab Republic Al-Kandari (2006) (52) Cross-sectional 20+ O N Kuwait Lafta & Kadhim (2005) Cross-sectional 7-13 O N Iraq (53) Al-Lawati & Jousilahti Cross-sectional 18+ O Y Oman (2004) (54)

766 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد العارش

Table 1 Summary of literature search (Concluded) Study (Year) (reference) Study design Age groupa Nutrition Western diet Region/Country/Territory (years) (N) or (Yes/No) Obesity (O) or Both (B) Abdul-Rahim et al. (2003) Cross-sectional 30+ O N Palestine (55) Galal (2003) (56) Analysis Children & N N MENA region adults Musaiger (2002) (57) Report 18+ N Y MENA region Benjelloun (2002) (58) Analysis Children & N N Morocco adults Galal (2002) (59) Analysis Children & N N Egypt adults Mokhtar et al. (2001) (60) Cross-sectional Children & B N Tunisia, Morocco adults Ba (2000) (61) Cross-sectional 18+ O N Mauritania Musaiger (1998) (62) Report 18+ N Y Bahrain, Kuwait, Oman, Qatar, Saudi Arabia, UAE Miladi & Musaiger (1998) Report 18+ N N MENA region (63)

aChildren and adults refers to studies that included population-level review data. All papers/studies reported a dietary shift away from traditional dietary practices and a correlation between the dietary shift and overweight/obesity. MENA = Middle East and North Africa; UAE = United Arab Emirates.

expand on the results of this study. Fi- This review was limited to 9 elec- and ageing adults, with consistent agree- nally, given that the time frame studied tronic biomedical databases, additional ment, to reduce variance within groups. represents less than a single generation, databases could have added to the study In addition, only sources published or retrospective longitudinal studies are in both complexity and sample size. Ad- made available in English were used warranted. ditionally, age groups described within for this study. Arabic, French and other The recent peer-reviewed studies individual articles overlapped; some language searches were excluded and offer insight into the increase of obe- child groups included ages 5 to 18 years therefore some relevant literature might sity in the MENA region. The studies while others used more narrow defini- have been missed. identified acknowledge that obesity is tions. None of the age subgroups identi- increasingly prevalent and problem- fied by individual sample publications atic among MENA countries. There is occurred with enough frequency and Conclusion a need add to obesity-related research consistency to allow for statistical analy- in Arab countries where correlational sis. Ideally, the research sample would Given that this study looked at obe- factors are identified and prevention is include carefully defined groups for chil- sity and not prevention, further effort discussed (24). dren, adolescents, young adults, adults, needs to be made by Arabic-speaking

Table 2 Number of studies showing obesity prevalence and dietary shift in different age groups Age groupa Obesity Westernized diet Significant Region/Country/Territory with prevalent with shift correlation significant correlation dietary shift Children (n = 11) 9 7 5 Bahrain, Egypt, Islamic Republic of Iran, Jordan, Kuwait, Lebanon, Oman, Saudi Arabia, Sudan and Turkey Adults (n = 16) 12 8 5 Bahrain, Kuwait, Qatar, Oman, Saudi Arabia, Lebanon, Libya, and United Arab Emirates Children and adults (n = 12) 5 4 2 Middle East and North Africa region

aChildren = 5-18 years; adults = 18 years and older, children and adults include all age ranges.

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countries to reduce obesity with spe- dietary guidelines for Americans but ap- health professionals, nutritionists and cial consideration given to preventive plicable for the Saudi population (27). dietitians and health educators should proposals and dietary interventions. A The WHO Regional Office published expect some predictable outcomes potential next phase is to concentrate a new dietary guideline and recommen- (32). Preventing these shifts is unlikely research efforts on developing public dations for an overall healthy pattern of (9,10,33) and acknowledging the po- health dietary strategies, interventions, eating that can be adopted among Arab tential and expected outcomes should and guidelines that are both age- and countries (28). It is compatible with be a priority. The Healthy Food Palm culturally-relevant to this region. A re- the various cultures and eating patterns Guide, The Arab Food Dome, dietary cently published recommendation by within the populations of the region and guidelines of the WHO Regional Office, is based on the availability of local foods Musaiger offered a unique culturally education on preparation of traditional traditionally consumed. compatible dietary guideline, the Arab healthy foods and eating habits, public Food Dome, designed for Arab coun- Traditionally, the Mediterranean re- health promotion of indigenous foods tries with food groups common to the gion has protected against overweight, and culturally relevant dietary habits are Mediterranean diet and specific to the obesity and their co-morbidities by its important therefore to help reduce the MENA region (25,26). Similar to the well documented and culture-specific risk of obesity within Arabic-speaking Arab Food Dome, the Saudi Ministry of dietary patterns (29–31). However, Health has published dietary guidelines, as developing countries shift from populations. the Healthy Food Palm, based on the traditional dietary patterns to adopt Funding: None. US Food and Drug Administration Westernized diet patterns, public Competing interests: None declared.

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WHO events addressing public health priorities

Intercountry meeting on controlled medicines 1

Introduction of pain management within health care services, inadequate Pharmaceutical preparations containing internationally con- education on narcotic medicines and psychotropic substances, trolled substances play an essential role in medical treatment exaggerated fear of opioids and addiction, and problems in the to relieve pain and suffering. Psychotropic substances such as supply chain for obtaining narcotic medications. benzodiazepine-type anxiolytics, sedative-hypnotics and bar- Participants recognized the barriers to opioid medication biturates are indispensable medications for the treatment of availability, which are multifactorial in nature. Therefore, neurological and mental disorders. Most narcotic medicines tackling the problem from the health side only will not ad- and psychotropic substances controlled under international dress the issue entirely. The main barriers identified by the drug control treaties are indispensable in medical practice. participants were legal and regulatory barriers, policy barriers, Opioid analgesics, such as codeine and morphine, as well as knowledge and societal attitudes, and economic aspects, semi-synthetic and synthetic opioids, are essential medicines for the treatment of pain and are listed on the WHO’s Model including affordability. List of Essential Medicines. Participants noted that governments need to enable and The WHO Eastern Mediterranean Region (EMR) has empower health care professionals to prescribe, dispense and extremely low consumption of controlled medicines as administer opioid medications in line with WHO policy direc- compared with other regions. This reflects a reality observed tions and treatment guidelines to meet the individual medical in various settings, where patients suffer from moderate to needs of patients. They must also ensure that sufficient supply severe pain which remains untreated, partly due to limited is available to meet those needs. access to strong analgesics. It was also noted that the governments have a dual obliga- An intercountry meeting on controlled medicines was tion to improve access to such medicines based on legal, hosted by the WHO Regional Office for the Eastern Medi- political, public health and moral grounds and have the obli- terranean in Cairo from 17 to 19 May 2016, involving 17 gation to protect populations against abuse and dependence. participants from 8 countries: Egypt, Islamic Republic of Iran, Therefore, a national policy should include the establishment Jordan, Lebanon, Oman, Saudi Arabia, Kuwait and Tunisia of a drug control system that prevents diversion and ensures and facilitated by WHO staff and international experts. adequate availability for medical use. The overall objective of the meeting was to address the very low consumption of controlled medicines for medical Accurate estimation of need is essential to ensure ad- use in the EMR. equate supply. The participants developed action plans for con- ducting country assessments using WHO country assessment Conclusions checklist. The main components of the action plans included Participants emphasized the importance of addressing the the establishment of a multi-sectoral committee for narcotics low availability and accessibility of narcotic medicines and and psychotropics, mapping of the current status, revising and psychotropic substances which are critical for pain manage- updating laws and guidelines concerned with the medical use ment of cancer, HIV/AIDS, injuries, surgical interventions and research of controlled medicines, integrating palliative care and obstructed labour, and for neurological and mental dis- orders. Ministries of health alone have limitations regarding services as part of the national health strategy, including pallia- access to information and impact on policy formulation. This tive care in health sciences’ curricula and in continuous medical is because the responsibility for overseeing law enforcement education, raising awareness of patients through campaigns, lies within different government bodies. and improving accuracy of estimation of controlled medicine It was understood that policy change alone does not bring needs in comparison with current requirements reported to the about increased access. There is a need to address the low priority International Narcotics Control Board.

1 This report is extracted from the Summary report on the Intercountry meeting on controlled medicines, Cairo, Egypt 19–17 May 2016 (http://applications.emro.who.int/docs/IC_Meet_Rep_2016_EN_18963.pdf?ua=1)

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