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

The theme for Universal Health Coverage Day on 12 December 2020 is “Protect Everyone”, emphasizing global and individual health security in the context of the COVID-19 pandemic – the causative agent of which (SARS-COV2) has been implicated to infect more than 4 million people in the Eastern Mediterranean Region. More than ever, Universal Health Coverage is a priority agenda of policy-makers and practitioners in the Region in order to save lives, advance health and protect livelihoods.

المجلد السادس والعشرون / عدد Volume 26 / No. 12 2020 12 ديسمبر/كانون األول December/Décembre Vol. 26.12 – 2020

Editorial ‘Health for All by All’ during a pandemic: ‘Protect Everyone’ and ‘Keep the Promise’ of Universal Health Coverage in the Eastern Mediterranean Region Awad Mataria, Richard Brennan, Arash Rashidian, Yvan Hutin, Asmus Hammerich, Maha El-Adawy and Rana Hajjeh...... 1436 Commentaries Why is COVID-19 more deadly among physicians than other health-care workers in the Islamic Republic of Iran? Kamran B. Lankarani...... 1440 Early responses to COVID-19 in Afghanistan Shugufa Basij-Rasikh, Merette Khalil and Najibullah Safi...... 1442 Research articles Knowledge, attitudes and practices towards COVID-19 among Pakistani residents: information access and low literacy vulnerabilities Zafar Fatmi, Shafaq Mahmood, Waqas Hameed, Ibtisam Qazi, Muhammad Muneebullah Siddiqui, Anny Dhanwani and Sameen Siddiqi...... 1446 Compliance with design principles: a case study of a widely used laboratory information system Zhila Agharezaei, Reza Khajouei, Leila Ahmadian and Laleh Agharezaei...... 1456 Predicted 10-year risk of cardiovascular disease in Islamic Republic of Iran and the body mass index paradox Mohammad Hassan Emamian, Hassan Hashemi and Akbar Fotouhi...... 1465 Workplace violence among health-care workers in emergency departments of public hospitals in Dammam, Saudi Arabia Moussa Harthi, Mohammed Olayan, Hassan Abugad and Moataza Abdel Wahab...... 1473 Access to health care for patients with thalassaemia in Greece: a cross-sectional study Kyriakos Souliotis, Christina Golna, Sofia Nikolaidi, Georgia Vatheia and Stanimir Hasurdjiev ...... 1482 Factors affecting hookah tobacco among females in the Islamic Republic of Iran: a qualitative study Mohammad Rafi Bazrafshan, Amir Mansouri, Hamed Delam, Behnam Masmouei and Nasrin Shokrpour...... 1493 Eating disorders among Jordanian adolescents with and without dysglycaemia: a comparative study Huda M. Al Hourani, Rana Ababneh, Nahla Khawaja, Yousef Khader and Kamel Ajlouni...... 1502 Does socioeconomic status influence oral cancer awareness? The role of public education Somayyeh Azimi, Zahra Ghorbani, Erfan Ghasemi, Marc Tennant and Estie Kruger...... 1510 Tobacco price increase and consumption behaviour among male smokers in Saudi Arabia: a community-based study Mohamad Al-Tannir, Amani Abu-Shaheen, Youssef Altannir and Mustafa Altannir...... 1518 Relative risk of injury due to alcohol consumption in car and motorcycle drivers Mahnaz Yadollahi and Forough Pazhuheian...... 1525 Geographic risk of general and abdominal obesity and related determinants in Iranian children and adolescents: CASPIAN-IV Study Maryam Yazd, Roya Kelishadi, Volker Schmid, Mohammad-Esmaeil Motlagh, Ramin Heshmat and Marjan Mansourian...... 1532

Eastern Mediterranean La Revue de Santé de la Health Journal Méditerranée orientale Views of community pharmacists in Lebanon on the unified prescription: a mixed method study Hani Dimassi, Aline Maroun, Marguerita Saadeh, Joanne Khabsa, Jessica-Lynn Abdou and Shadi Saleh...... 1539 Identification of immunoreactive proteins in secretions ofLeishmania infantum promastigotes: an immunoproteomic approach Sajad Rashidi, Paul Nguewa, Zahra Mojtahedi, Bahador Shahriari, Kurosh Kalantar and Gholamreza Hatam...... 1548 National food policies in the Islamic Republic of Iran aimed at control and prevention of noncommunicable diseases Masoumeh Moslemi, Mehrnaz Kheirandish, Nezhad Fard Ramin Mazaheri, Hedayat Hosseini, Behrooz Jannat, Vahid Mofid, Moghaddam Atefeh Fooladi and Nader Khosroshahi Karimian...... 1556 Review The status of cryptosporidiosis in Jordan: a review AbdelRahman Zueter...... 1565 Short research communication Implementing the Health Early Warning System based on syndromic and event-based surveillance at the 2019 Hajj Kingsley Lezor Bieh, Anas Khan, Saber Yezli, Ahmed El-Ganainy, Sari Asiri, Badriah Alotaibi, Sujoud Ghallab, Amgad Elkholy, Abdinasir Abubakar and Hani Jokhdar ...... 1570 WHO events addressing public health priorities Elimination of neglected tropical diseases under preventive chemotherapy programmes in the Eastern Mediterranean Region...... 1576 Ahmed Al-Mandhari Editor-in-Chief Arash Rashidian Executive Editor Ahmed Mandil Deputy Executive Editor Phillip Dingwall Managing Editor

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

Editorial assistants Nadia Abu-Saleh, Suhaib Al Asbahi (graphics), Diana Tawadros (graphics)

Editorial support Guy Penet (French editor) Eva Abdin, Fiona Curlet, Cathel Kerr, Marie-France Roux (Technical editors) Ahmed Bahnassy, Abbas Rahimiforoushani, Manar El Sheikh Abdelrahman (Statistics editors)

Administration Iman Fawzy, Marwa Madi

Web publishing Nahed El Shazly, Ihab Fouad, Hazem Sakr

Library and printing support Hatem Nour El Din, Gehane Al Garraya, Metry Al Ashkar, John Badawi, Ahmed Magdy, Amin El Sayed

Cover and internal layout designed by Diana Tawadros and Suhaib Al Asbahi Printed by WHO Regional Office for the Eastern Mediterranean, Cairo, Egypt Editorial EMHJ – Vol. 26 No. 12 – 2020

‘Health for All by All’ during a pandemic: ‘Protect Everyone’ and ‘Keep the Promise’ of Universal Health Coverage in the Eastern Mediterranean Region

Awad Mataria,1 Richard Brennan,2 Arash Rashidian,3 Yvan Hutin,4 Asmus Hammerich,5 Maha El-Adawy 6 and Rana Hajjeh 7

1Director, Department for Universal Health Coverage/Health Systems, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. 2Regional Emergency Director, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt.3 Director, Depart- ment for Science, Information and Dissemination, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt.4 Director, Department for Universal Health Coverage/Communicable Diseases, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. 5Director, Department for Universal Health Coverage/Noncommunicable Diseases and Mental Health, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt.6 Director, Department for Health Protection and Promotion, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt.7 Director of Programme Management, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. (Correspondence to: Awad Mataria: [email protected]). Citation: Mataria A; Brennan R; Rashidian A; Hutin Y; Hammerich A; El-Adawy M; et al. ‘Health for All by All’ during a pandemic: ‘Protect Everyone’ and ‘Keep the Promise’ of Universal Health Coverage in the Eastern Mediterranean Region. East Mediterr Health J. 2020;26(12):1436–1439. https://doi. org/10.26719/2020.26.12.1436 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo)

The Universal Health Coverage (UHC) Day has been the EMR was estimated at 58 (out of 100) in 2019, below commemorated on 12 December every year since 2017 the global average of 66 (out of 100), and behind three (1). In 2019, the theme of the day was “Keep the Promise”, other WHO Regions (12). Close to 77 million people in referring to the Political Declaration on UHC endorsed by the EMR faced financial hardship in 2015 by spending Heads of States at the United Nations General Assembly more than 10% of their resources as direct out-of-pocket High-Level Meeting on 23 September 2019 (2). In 2020, payments – 15 million more compared with 2010 (13). the theme is “Protect Everyone”, emphasizing global These overall indices reflect difficulties in provision of and individual health security in the context of the care to key subgroups, countries and geographical areas COVID-19 pandemic, attributed to SARS-CoV 2 – a virus in the Region. Several vulnerable groups in the EMR that infected more than 4 million people in the Eastern remain uncovered by financial protection or without Mediterranean Region (EMR) and left over 100 000 dead access to their needed quality health care – including in less than 12 months (6.6% and 7.1% of the global toll, communities impacted by conflict and state fragility, respectively) (3). Keeping the promise of UHC, while refugees, migrants and those in the informal sector ensuring health security, is becoming a priority agenda (14). The COVID-19 pandemic has amplified all these of policy-makers and practitioners in the EMR in order challenges (15). to save lives, advance health and protect livelihoods (4). Protecting everyone: where are we in the Eastern Covering everyone: where are we in the Eastern Mediterranean Region? Mediterranean Region? Health security is about reducing vulnerability to Universal health coverage is about ensuring that all health threats at individual and collective levels (16). The individuals and communities have access to their EMR is prone to emergencies from multiple hazards, needed health services of good quality and with financial including disease outbreaks, natural disasters, conflicts, protection (5). Primary Health Care (PHC) is recognized displacements, and technological disasters. Of particular as the most inclusive, effective and efficient approach to concern are the multiple conflicts and humanitarian promote health and achieve UHC (6). The EMR was the first crises across the Region, where major health system WHO region to express collective political commitment disruptions pose enormous obstacles to health service towards UHC by signing the UHC2030’s Global Compact delivery and health security (17). Over 69.6 million people (7) and endorsing the 2018 Salalah Declaration (8). The living in the Region require humanitarian assistance, latter provides a regional roadmap based on PHC to achieve representing 42% of the global total (18). The Region is UHC by 2030 (9). Nevertheless, in 2019 the UHC Global also source of 64% of the world’s refugees, many of whom Monitoring Report (10) showed that the EMR is lagging remain in the EMR (19). behind in achieving the UHC targets of the Sustainable Between 2016 and 2018, Joint External Evaluations Development Goals (SDGs): Service Coverage (SDG (JEEs) (20) assessed 18 EMR countries in terms of their target 3.8.1) and Financial Protection (SDG target 3.8.2). ability to prevent, prepare for, detect and respond to Countries in the EMR face a plethora of public health public health risks, as pertains to International Health challenges: from high rates of smoking to high intake of Regulations’ implementation (21). The evaluations sugar and salt, emerging and re-emerging communicable revealed varying levels of capacities. Accordingly, National diseases, weak disease surveillance and response, and the Action Plans for Health Security were developed but not unfinished agenda in many countries of high maternal adequately implemented. The response to COVID-19 and child mortality (11). The Service Coverage Index in pandemic has exposed additional gaps in emergency

1436 Editorial EMHJ – Vol. 26 No. 12 – 2020 preparedness and management across the Region that for a paradigm shift towards developing resilient health the JEEs did not fully reveal. After almost one year of the systems that ensure health security while advancing UHC pandemic, the most pressing challenges continue to exist based on the PHC approach. The ‘Step 0’ in health system – scaling up proven public health measures, tackling recovery from COVID-19 requires adequate investment COVID-19 fatigue, balancing the easing of COVID-19 in Essential Public Health Functions and other Common control measures while maintaining suppression of Goods for Health (e.g. policy and coordination, taxes the virus transmission, and establishing a platform for and subsidies, regulations and legislations, information, distribution of COVID-19 vaccines (22). analysis and communication and population services) Universal Health Coverage and Health Security – lessons (30), coupled with rebuilding ‘fit-for-purpose’ institutions from COVID-19 for the Eastern Mediterranean Region towards UHC and health security (31). This calls for integrating health programs’ specificities; e.g. Dr Adhanom Ghebreyesus Tedros, World Health communicable diseases, noncommunicable diseases, Organization (WHO) Director-General, has repeatedly mental health, and reproductive, maternal, neonatal, indicated that UHC and Health Security are two sides of child and adolescent health, in all endeavors that aim for the same coin (23). COVID-19 unveiled how ill-prepared strengthening health systems. the world was to face a pandemic of such magnitude and how vulnerable most national health systems are to What is needed to protect everyone and keep the ensure continuous access to essential health services amid promise of Universal Health coverage in the Eastern emergencies. A survey conducted in the EMR revealed Mediterranean Region? that about 75% of essential health services had some level Advancing UHC and ensuring health security are two key of disruption (in 13 out of 22 countries that responded), Regional Strategic Priorities in the EMR Vision 2023 (32). mostly affecting routine immunizations, dental services, Moving ahead requires building resilient health systems rehabilitation services, and family planning, in addition that are able to resist, absorb, accommodate and recover to chronic disease management, including cancer care from external shocks in a timely and efficient manner (16). (22). Moreover, the pandemic has exposed the fragility of The ‘Turning Vision into Action’ paper (33) endorsed by medicine and vaccine supply chains. the 66th Session of Eastern Mediterranean Regional The pandemic is projected to cost the world up to US$ 21 Committee in 2019 identified the Strategic Directions to trillion; a cost which could have been largely avoided with advance the complementary goals of UHC and Health an adequate investment in emergency preparedness (24). Security. Prominent among those are: investing in health The pandemic has demonstrated the value of decisive protection and promotion, evidence-informed policy- and collaborative leadership based on evidence-informed making (34), building effective information systems decisions (25). It has also highlighted more than ever the (35) and disease surveillance approaches, strengthening importance of whole-of-society, whole-of-government emergency preparedness and response, investing approaches in formulating policies and ensuring their in health workforce and facilitating community effective implementation. Furthermore, it reminded us engagement. Sustainability can only be ensured by of the key role of health professionals, stressing their institution building. chronic universal shortages as previously reiterated by We have always known that diseases have no the High-Level Commission on Health Employment and borders and that only collective efforts ensure the Economic Growth (26). Finally, the pandemic signaled safety and security of all. A pandemic is not the time to the low investment in Essential Public Health Functions stall investments in public health. Just the opposite. As (27) and other Common Goods for Health in building we respond to COVID-19, countries must invest more equitable and resilient health systems (28). and invest better in strong health systems to ‘Protect How to build a resilient health system that supports Everyone’ – during and after the pandemic. This the dual goal of Universal Health Coverage and Health should include the young and the old, men and women, Security? citizens and residents, refugees, migrants and internally The concept of “health system strengthening” made its displaced people, etc. WHO together with all health and way to global public health in the last few decades as key development partners shall continue to build and rebuild for the effective implementation of global and national health systems to achieve UHC and Health Security, via health policies. Health systems mean ‘all institutions technical cooperation, capacity building and experience and activities whose primary purpose is to promote, sharing. ‘Health for All by All’ has been the regional motto maintain or restore health’ (29). COVID-19 unveiled gaps since 2018. COVID-19 has underscored its relevance today in current health systems analytical approaches, calling more than ever.

1437 Editorial EMHJ – Vol. 26 No. 12 – 2020

References 1. United Nations. International Universal Health Coverage Day. New York: United Nations; 2019 (https://universalhealthcoverage- day.org/). 2. United Nations. Universal Health Coverage: moving together to build a healthier world – UN high-level meeting on Universal Health Coverage. New York: United Nations; 2019 (https://www.un.org/pga/73/event/universal-health-coverage/). 3. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Eastern Mediterranean Regional Office COVID-19 dashboard. Cairo: WHO/EMRO; 2020 (https://app.powerbi.com/view?r=eyJrIjoiN2ExNWI3ZGQtZDk3My00Yz- E2LWFjYmQtNGMwZjk0OWQ1MjFhIiwidCI6ImY2MTBjMGI3LWJkMjQtNGIzOS04MTBiLTNkYzI4MGFmYjU5MCIsImMiO- jh9). 4. Al-Mandhari A. Public health in the Eastern Mediterranean Region: profound challenges, huge opportunities. Lancet. 2019 Sep 21;394(10203):992-993. doi:10.1016/S0140-6736(19)32138-5. 5. World Health Organization. Universal health coverage (UHC). Geneva: World Health Organization; 2019 (https://www.who.int/ news-room/fact-sheets/detail/universal-health-coverage-(uhc)). 6. World Health Organization and the United Nations Children’s Fund (UNICEF). Declaration of Astana. Geneva: WHO & UNICEF; 2018 (https://www.who.int/docs/default-source/primary-health/declaration/gcphc-declaration.pdf). 7. UHC2030. Global compact. Geneva & New York: World Health Organization; 2020 (https://www.uhc2030.org/what-we-do/working-better-together/global-compact/). 8. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Salalah Declaration signals countries’ firm commitment to universal health coverage. Cairo: WHO/EMRO; 2018 (http://www.emro.who.int/media/news/salalah-decla- ration-signals-countries-firm-commitment-to-universal-health-coverage.html). 9. Al-Mandhari A. Achieving “Health for All by All” in the Eastern Mediterranean Region. East Mediterr Health J. 2019 Oct 13;25(9):595-596. https://doi.org/10.26719/2019.25.9.595. 10. World Health Organization. Health statistics and information systems. Geneva: World Health Organization; 2020 (https://www. who.int/healthinfo/universal_health_coverage/report/2019/en/). 11. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Country health profiles. Cairo: WHO/ EMRO; 2020 (http://www.emro.who.int/entity/statistics/country-health-profiles.html). 12. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Monitoring health and health system performance in the Eastern Mediterranean Region. Cairo: WHO/EMRO; 2019 (https://rho.emro.who.int/sites/default/files/book- lets/EMR-HIS-and-core-indicators-2019-final_0.pdf%20). 13. World Health Organization. Health statistics and information systems – 2019 monitoring report. Geneva: World Health Organi- zation; 2020 (https://www.who.int/healthinfo/universal_health_coverage/report/2019/en/). 14. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Regional committee technical papers. Cairo: WHO/EMRO; 2018 (https://applications.emro.who.int/docs/RC_Technical_Papers_2018_4_20534_EN.pdf?ua=1). 15. Al-Mandhari A. Coming together in the Region to tackle COVID-19. East Mediterr Health J. 2020 Sep 24;26(9):992-993. https://doi. org/10.26719/2020.26.9.992 16. Kutzin K, Sparkes S. Health systems strengthening, universal health coverage, health security and resilience. Bull World Health Organ. 2016;94:2 http://dx.doi.org/10.2471/BLT.15.165050 17. Brennan R, Hajjeh R, Al-Mandhari A. Responding to health emergencies in the Eastern Mediterranean region in times of con- flict. Lancet 2020(2 March). https://doi.org/10.1016/S0140-6736(20)30069-6 (Epub ahead of print). 18. United Nations Office for the Coordination of Humanitarian Affairs (OCHA). Global humanitarian overview 2020. New York: OCHA; 2019 (https://www.unocha.org/sites/unocha/files/GHO-2020_v9.1.pdf). 19. United Nations High commissioner for Refugees (UNHCR). UNHCR global trends—forced displacement in 2018. Geneva: UN- HCR; (https://www.unhcr.org/5d08d7ee7.pdf). 20. World Health Organization. Strengthening health security by implementing the International Health Regulations (2005) – Joint External Evaluations. Geneva: World Health Organization; 2020 (https://www.who.int/ihr/procedures/joint-external-evaluations/ en/0. 21. World Health Organization. International Health Regulations (2005). Geneva: World Health Organization; 2020 (https://www.who.int/publications/i/item/9789241580410). 22. Al-Mandhari AS, Brennan RJ, Abubakar A, Hajjeh R. Tackling COVID-19 in the Eastern Mediterranean Region. Lancet. 2020(19 November). https://doi.org/10.1016/ S0140-6736(20)32349-7 (In press). 23. Tedros AG. All roads lead to universal health coverage. Geneva: World Health Organization; 2017 (http://www.who.int/news- room/commentaries/detail/all-roads-lead-to-universal-health-coverage). 24. World Health Organization. A world in disorder: Global Preparedness Monitoring Board annual report 2020. Geneva: World Health Organization; 2020 (https://apps.who.int/gpmb/assets/annual_report/GPMB_AR_2020_EN.pdf). 25. Obaid Al Saidi AM, Abikar Nur F, Al-Mandhari AS, El Rabbat M, Hafeez A, Abubakar A. Decisive leadership is a necessity in the COVID-19 response. Lancet 2020;396(10247): 295–98 (https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7333999/).

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26. World Health Organization. Health workforce – high-level commission on health employment and economic growth. Geneva: World Health Organization; 2016 (https://www.who.int/hrh/com-heeg/en/). 27. Alwan A, Shideed O, Siddiqi S. Essential public health functions: the experience of the Eastern Mediterranean Region. East Medi- terr Health J. 2016 Dec 12;22(9):694-700. https://doi.org/10.26719/2016.22.9.694. 28. Soucat A, Kickbusch I. Global common goods for health: towards a new framework for global financing. Global Policy. 2020;11(5):628-635 (https://onlinelibrary.wiley.com/doi/epdf/10.1111/1758-5899.12875). 29. World Health Organization. The world health report 2000. Geneva: World Health Organization; 2000 (https://www.who.int/ whr/2000/en/whr00_en.pdf?ua=1). 30. Soucat A. Financing common goods for health: fundamental for health, the foundation for UHC. Health Systems and Reform. 2019;5(4) (https://www.tandfonline.com/doi/full/10.1080/23288604.2019.1671125). 31. UHC2030. Living with COVID-19: Time to get our act together on health emergencies and UHC. Geneva: World Health Organ- ization; 2020 (https://www.uhc2030.org/fileadmin/uploads/uhc2030/Documents/Key_Issues/Health_emergencies_and_UHC/ UHC2030_discussion_paper_on_health_emergencies_and_UHC_-_May_2020.pdf). 32. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO. Vision 2023 Eastern Mediterranean Region. Cairo: WHO/EMRO; 2018 (http://www.emro.who.int/about-who/vision2023/vision-2023.html). 33. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO. WHO’s strategy for the Eastern Medi- terranean Region, 2020-2023. Cairo: WHO/EMRO; 2019 (https://applications.emro.who.int/docs/EMRPUB-RDO-014-2019-EN.pdf). 34. Rashidian A, Mandil A, Mahjour J. Improving evidence informed policy-making for health in the Eastern Mediterranean Region. East Mediterr Health J. 2018;23(12):793-794. https://doi.org/10.26719/2017.23.10.793 35. Rashidian A. Effective health information systems for delivering the Sustainable Development Goals and the universal health coverage agenda. East Mediterr Health J. 2019;25(12):849-851. https://doi.org/10.26719/2019.25.12.849

1439 Commentary EMHJ – Vol. 26 No. 12 – 2020

Why is COVID-19 more deadly among physicians than other health- care workers in the Islamic Republic of Iran?

Kamran B. Lankarani 1

1Health Policy Research Center, Institute of Health, Shiraz University of Medical Sciences, Islamic Republic of Iran. (Correspondence to: Kamran B. Lankarani: [email protected]).

Citation: Lankarani KB. Why is COVID-19 more deadly among physicians than other health-care workers in the Islamic Republic of Iran? East Mediterr Health J. 2020;26(12):1440–1441. https://doi.org/10.26719/emhj.20.134 Received: 27/07/20; accepted: 19/10/20 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

A report by Amnesty international released 13 July 2020 in inconsiderate use of PPE. Despite good knowledge on announced that more than 3000 health-care workers had infection control practices, the real observation of these died due to infection with SARS-CoV-2 since the begin- safety measures by physicians in practice might be as low ning of the current pandemic (1). The highest death toll as 3-26% (6,7). was from the Russian federation with 545 deaths, fol- While most hospitals in the Islamic Republic of Iran lowed closely by the United Kingdom and United States now provide PPE to all staff, the situation in out-patient of America with 540 and 507 fatalities, respectively. The departments, public or private, is not the comparable. report suggests these high figures are probably an under- There are more examples of negligence in following reporting of the true statistics. For example, the numbers appropriate precautions in out-patient departments, in the United States alone are believed to be more than such as non-observance of physical distancing resulting 800 as of July 2020 (2). While a major concern in some in crowded clinics increasing the risk of transmission. of these countries are disparities in the death toll among By contrast, it is much more feasible to observe physical ethnic minorities with disproportionately higher death distancing in hospitals with their no visitor policies. rates among black, Asian and minority ethnic (BAME) Symptomatic patients arriving at clinics with atypical physicians (3), the case in the Islamic Republic of Iran ap- extra pulmonary manifestations may result in reduced pears different. observation of standard precautions by physicians, According to data from the Islamic Republic of Iran who consider their patients not having COVID-19. It Medical Council, 138 health-care workers in the Islamic is significant that several Iranian physicians who died Republic of Iran had died due to COVID-19 (23 July from COVID-19 were not involved in hospital care of 2020) (4). While nursing staff constituted nearly 20% of infected patients, including physicians from disciplines the fatalities, another 20% were those working in other such as ear nose and throat and ophthalmology, but had hospital services, as well as health technicians working confirmed exposure to infected patients with atypical in the primary health care system. However, nearly 60% symptoms such as anosmia or conjunctivitis. More of those who died were physicians, of whom 28% were than 10% of Iranian gastroenterologists were found to general practitioners and 32% were specialists. This is in have symptomatic COVID-19 in the early phase of the contrast to data from the United Kingdom where nurse pandemic during late March 2020 (8). This high number fatalities outnumbered that of physicians (5). could be related to the fact that up to 50% of SARS- Although the death of any health worker is a tragic loss, CoV-2 infected patients may have had gastrointestinal especially in the middle of a pandemic, the significant complaints, even without respiratory symptoms, at the proportion of physicians dying from COVID-19 needs onset of the disease. In addition, many physicians can be special attention. negligent of their own health, resulting in a delay before A number of countries have raised concerns over seeking medical care, yet continue working despite the the availability of personal protective equipment (PPE). need for hospitalization or at least rest (9). However, this could not explain the disproportionate Moreover, the concerns over airborne transmission number of deaths of Iranian physicians. When of SARS-CoV-2 outside of medical procedures have made considering that the exposure time of nurses to COVID-19 the situation even more challenging. Any contact without patients in hospitals, specifically in intensive care units, proper physical distancing or in closed unventilated space is several times greater than physicians, and yet both have could potentially increase the chance of transmittance the same access to PPE, then other factors are implicated. of SARS-CoV-2. Added to this is the fact that any health- One factor may be the careless use of PPE by physicians. care worker fatality not only reduces available human There is greater discipline to follow safety procedures resources needed to confront the pandemic, but also in nursing, likely due to the presence of supervisors affects the mental health of remaining staff, reducing observing their activities. This is not the case for most their capacities to carry out their work effectively, and physicians, especially senior grades, possibly resulting disrupting family life. This issue needs to be taken

1440 Commentary EMHJ – Vol. 26 No. 12 – 2020 seriously and health systems should have a programme their proper use is of the utmost importance, the practice in place for the safety of their staff. of hand hygiene and approach that all patients and visitors could be potentially infected should encourage In conclusion, Iranian physicians appear to be at a physicians to follow strict infection prevention measures. higher risk of death due to COVID-19. There are several Specific programmes to encourage the monitoring and suggested explanations for this disproportionately support of health-care workers would address many of the higher rate, and effective measures for all health workers, risks mentioned, with a particular focus on physicians, including physicians, should be enacted through a who have been observed to be particularly negligent over systematic approach (10). While availability of PPE and their own health.

References 1. Amnesty International. Exposed, silenced, attacked: failures to protect health and essential workers during the COVID-19 pan- demic, 2020 (https://www.amnesty.org/en/documents/pol40/2572/2020/en/, accessed 23 July 2020) 2. The Guardian. Covid-19 healthcare worker death toll: 821 deaths under investigation. The Guardian, 23 July, 2020 (https://www. theguardian.com/us-news/2020/jun/17/covid-19-coronavirus-healthcare-workers-deaths, accessd 23 July 2020) 3. Kursumovic E, Lennane S, Cook TM. Deaths in healthcare workers due to COVID-19: the need for robust data and analysis. An- aesthesia. 2020;75(8):989-92. 4. Tehran Times. Coronavirus: 138 healthcare workers in Iran lose lives. Tehran Times, 22 July 2020 (https://www.tehrantimes.com/ news/450361/Coronavirus-138-healthcare-workers-in-Iran-lose-lives, accessed 23 July 2020). 5. Cook T, Kursumovic E, Lennane S. Exclusive: deaths of NHS staff from covid-19 analysed. Health Service Journal. 22 April 2020 (https://www.hsj.co.uk/exclusive-deaths-of-nhs-staff-from-covid-19-analysed/7027471.article, accessed 23 July 2020). 6. Askarian M, Shiraly R, Aramesh K, McLaws ML. Knowledge, attitude, and practices regarding contact precautions among Irani- an physicians. Infect Control Hosp Epidemiol. 2006;27(8):868-72. 7. Nabavi M, Alavi-Moghaddam M, Gachkar L, Moeinian M. Knowledge, attitudes, and practices study on hand hygiene among Imam Hossein Hospital’s Residents in 2013. Iran Red Crescent Med J. 2015;17(10):e59542. 8. Hormati A, Niya MHK, Ghadir M, Lankarani KB, Ajdarkosh H, Tameshkel FS, et al. COVID-19 in the endoscopy ward: A potential risk for gastroenterologists. Infect Control Hosp Epidemiol. 2020:1-2. 9. Wong AMF. Beyond burnout: looking deeply into physician distress. Can J Ophthal. 2020;55(3, Supplement 1):7-16. 10. Hassan IS, Obaid F, Ahmed RA, Abdelrahman LS, Adam SA, Adam OI, et al. A Systems Thinking approach for responding to the COVID-19 pandemic. East Mediterr Health J. 2020 Aug 25;26(8):872-876. doi: 10.26719/emhj.20.090.

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Early responses to COVID-19 in Afghanistan

Shugufa Basij-Rasikh,1 Merette Khalil 2 and Najibullah Safi 1

1World Health Organization Country Office, Kabul, Afghanistan.2 World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. (Correspondence to: Merette Khalil: [email protected]).

Citation: Basij-Rasikh S; Khalil M; Safi N. Early responses to COVID-19 in Afghanistan. East Mediterr Health J. 2020;26(12):1442–1445. https://doi. org/10.26719/emhj.20.137 Received: 09/07/20; accepted: 29/10/20 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction crowds and upscale hand-hygiene were issued, and Min- istry of Interior Affairs (MoI) banned large gatherings, The World Health Organization (WHO) declared COV- sporting and entertainment events (2,12). Quarantine and ID-19 as a pandemic on 13 March 2020. It has spread to lockdown were implemented throughout the country more than 200 countries, with over 35 million cases and 1 (Figure 1) (2,13,14). Notably, the political changes in gov- million deaths, with no guaranteed treatment but recom- ernment and new minsters of health disrupted the na- mended preventive measures like hand hygiene and so- tional response to COVID-19 and resulted in policy mod- cial distancing (1). As a donor-dependent conflict-affected ifications, fragmentation and delays in implementation. country, Afghanistan faces challenges with health-care delivery and managing its double burden of diseases, giv- In March 2020, the MoPH developed the National en the limited health literacy and preventative measures, Emergency Response Plan for COVID-19, in collaboration shortages of skilled health workers, and fragile health with the World Health Organization (WHO) (13,15). The infrastructure (2,3). Afghanistan has a population of 32 government allocated 8 billion afghanis 1 (Afs) (0.5% of million; 75% live in the rural areas and 80% living below GDP) for emergency pandemic response, of which 1.9 the poverty line (4). Given Afghanistan’s close proximity billion afghanis (0.1% of GDP) for urgent health needs (6). to China, the Afghan Ministry of Public Health (MoPH) The government announced lockdown in three provinces began discussing preparedness measures for COVID-19 bordering the Islamic Republic of Iran due to surge in as early as December 2019 and predicted that 80% of the cases and all flights were suspended from Kabul 14( ). population could be infected with upward of 125 000 deaths in Kabul alone if preventative measures were not Role of media and communication followed (5–7). Collaboration with media and religious leaders was es- The first case of COVID-19 in Afghanistan was sential in assuaging panic in communities, combatting reported on 22 February 2020, when 150 000 nationals misinformation on the virus’ spread, and growing stig- returned from the Islamic Republic of Iran to Herat ma against the overburdened health system. MoPH and (8). More recently (5 October 2020), there were 39 422 Ministry of Communication and Technology Affairs confirmed cases, 32 879 recovered and 1466 deaths, and jointly developed a mobile application providing updates increasing (9,10). Kabul and Herat are the most affected on COVID-19 (9). The WHO emergency team launched parts of the country (9,11). Despite its fragile health a media campaign, conducted month-long roundtables, system and limited preparedness and surveillance and oriented 55 256 community and religious leaders in capacities, Afghanistan was among the first countries in all 34 provinces (13). Information Education and Commu- the Eastern Mediterranean Region and world to consider nication (IEC) materials were developed from the Islamic multisectoral and proactive preparedness measures in perspective (including a fatwa regarding COVID-19 pre- managing the COVID-19 outbreak. ventive measures), and distributed by Ministry of Reli- gious Affairs and WHO; further materials were prepared National interventions for those illiterate or have no access to internet (9,16,17). Measures to increase preparedness, detection and re- This was particularly important as the first wave of COV- sponse to COVID-19 were issued and implemented at a ID-19 coincided with numerous religious holidays where national scale starting January 2020, prior to the first case large gatherings and close physical contact would have being diagnosed in-country. One of the earliest measures been common and a potential spreader of the infection. included cross-border screenings at points of entry (Fig- Unfortunately, MoPH struggled to control communities’ ure 1); this was due to the surge of returnees from the Is- adherence to these preventive measures, especially giv- lamic Republic of Iran, which at the time was a hot-spot en the shortages of personal protection equipment (PPE) for COVID-19 cases. Presidential decrees to avoid large and the harsh economic conditions facing the country (5).

1 afghani = US$ 0.013 (29 October 2020)

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Health systems interventions There are total of 8996 medical doctors, 12 588 nurses and 26 696 midwives, resulting in a shortage In February 2020, the MoPH designated the Afghan Japan of skilled health workers nationally, and the issue of hospital in Kabul as an immediate COVID-19 treatment maldistribution since the majority are concentrated in facility (9). In Afghanistan, 1541 beds are designated for urban areas and some 60% work in public-health facilities COVID-19 patients, 700 beds in Herat, 200 beds in Kabul, (3). To respond to the COVID-19 pandemic, MoPH issued a and the remainder are spread around the country (9,11). call to recruit fresh graduates, volunteers, and registered In Kabul, Darulaman Palace and Kabul and Polytechnic medical professionals to work in designated hospitals. universities’ dormitories were converted into isolation In May 2020, 763 medical staff were trained on IPC and facilities. Isolation wards were identified for treatment case management (9,20). However, despite some financial of patient with COVID-19 in all provinces (9,11). By March incentives (hardship payments), it was difficult to retain 2020, there were 300 ICU beds available for quarantine many of these staff due to the challenging working throughout the country (11). conditions, high risk of infection, limited PPE, and Regarding service delivery, under the isolation ward inadequate training and experience in managing critical protocol, mild and moderate cases were to be quarantined cases (especially for new graduates). at home to allow severe cases to be monitored at the hospital (18). The role of private hospitals was neither Recommendations to improve the compulsory nor voluntary in COVID-19 response. Given COVID-19 response Afghanistan’s vertical and contracted-out health systems infrastructure, the provision of non-COVID-19 and The impact of COVID-19 on health, education and the essential health services was continued through NGOs, economy, especially in fragile contexts such as Afghani- utilizing additional triage and infection prevention and stan, is difficult to ignore. An evaluation of Afghanistan’s control (IPC) measures (19). experiences in combatting COVID-19 and the lessons learned from responses and interventions in the early Despite the increasing cases, Afghanistan had one months would benefit policy-makers at the national lev- of the lowest national testing capacities in the Region el as well as public health researchers and humanitarian for COVID-19; this challenge was exacerbated by the actors in similar settings. While Afghanistan has taken shortages of testing kits nationally, high costs of testing, many pro-active measures to prevent the transmission insecurity in transporting tests, and the need to export of the disease, further multi-sectoral policies would not samples abroad for confirmation and verification2,5,15 ( ). only improve the efficiency of the current response but By May 2020, there were a total of 9 certified laboratories may be proactively established ahead of a second wave with the capacity of 1790 tests per day (9). Additionally, (5); these include: Afghanistan decentralized its testing capacity. In addition to the Central Public Health Laboratory (CPHL) • Increasing budget allocation towards the health-care (processing 200-300 samples/day) and two veterinary sector to improve hospital facilities, proper staffing, laboratories in Kabul, there were also two laboratories in and procurement of required medical equipment; Herat (150 test/day), one in Nangarhar and one in Paktya, • scaling up capacity building of health-care Kandahar, and Balkh provinces, each testing about 100- professionals for use of PPE, IPC, rapid detection, case 150 COVID-19 cases daily (2,11,13,16). management, and critical care services; Despite the limited capacity to confirm and diagnose • recruiting additional health workers, and engaging the virus, Afghanistan stepped up its capacity for community health workers and community actors in identification and contact tracing through utilizing COVID-19 surveillance; existing surveillance infrastructure. Afghanistan used • expanding use of telehealth care and helpline services 520 sentinel sites in all the 34 provinces in both public to support service delivery while maintaining and private health facilities (11,13). In addition, active quarantine, particularly to improve access in rural surveillance sites have been established in all border- and remote areas; crossings around the country and involvement of polio • continuing health promotion activities, particularly workers and rapid response teams (RRTs) used to expand for illiterate and hard-to-reach populations, to raise contact tracing, sample collection, and risk communication awareness and increase use of preventive practices in insecure areas (16). Regarding equipment, supplies such as handwashing and using masks; and medicines, United Nations’ reports confirmed that due to the reliance on humanitarian and international • raising awareness to reduce myths and stigma organizations, Afghanistan had enough PPEs, masks and associated with COVID-19, through continued gloves available in the COVID-19 designated hospitals at media campaigns and engagement of religious and the beginning of the response, including approximately community leaders; 85 000 test kits and 600 ventilators throughout the • focusing on internally displaced populations and country (9). returnees to ensure adequate screening, health

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education, and access to health services; psychological support services in the service delivery • engaging with the private sector to expand and plan; and optimize service delivery, surveillance, laboratory capacity and prevention; • conducting scientific research on preventive • analyzing the psychological impact of COVID-19 measures and practices in rural and urban areas to on the population and incorporating therapy and limit the spread of infection.

References 1. World Health Organization. Coronavirus Disease (COVID-19) Dashboard. Geneva: World Health Organization; 2020 (https://cov- id19.who.int/). 2. Shah J, Karimzadeh S, Al-Ahdal TMA, Mousavi SH, Zahid SU, Huy NT. COVID-19: the current situation in Afghanistan. The Lan- cet Global Health. 2020 Apr 2. https://doi.org/10.1016/S2214-109X(20)30124-8 3. Safi N, Naeem A, Khalil M, Anwari P, Gedik G. Addressing health workforce shortages and maldistribution in Afghanistan. East Mediterr Health J. 2018;24(9):951–958. https://doi.org/10.26719/2018.24.9.951. 4. Afghanistan Humanitarian Needs Overview 2020 (December 2019) - Afghanistan. ReliefWeb. (https://reliefweb.int/report/af- ghanistan/afghanistan-humanitarian-needs-overview-2020-december-2019). 5. Mousavi SH, Abdi M, Zahid SU, Wardak K. Coronavirus disease 2019 (COVID-19) outbreak in Afghanistan: Measures and chal- lenges. Infect Control Hosp Epidemiol. 2020 May 15:1–2. 6. International Monetary Fund (IMF). Policy responses to COVID19 [Internet]. Policy Tracker COVID19. (https://www.imf.org/en/ Topics/imf-and-covid19/Policy-Responses-to-COVID-19). 7. United States Embassy. COVID Information. Kabul: United States Embassy; 2020 (https://af.usembassy.gov/covid-19-informa- tion/%3E). 8. Azizy A, Fayaz M, Agirbasli M. Do not forget Afghanistan in times of COVID-19: Telemedicine and the internet of things to strengthen planetary health systems. OMICS: A Journal of Integrative Biology. 2020:Apr 23 (https://www.liebertpub.com/doi/ full/10.1089/OMI.2020.0053). 9. World Health Organization. Coronavirus disease 2019 (COVID-19) Weekly Situation Report No. 15;5. Kabul: World Health Organ- ization; 2020. 10. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). COVID-19 Dashboard. Cairo: WHO/ EMRO: 2020 (https://app.powerbi.com/view?r=eyJrIjoiN2ExNWI3ZGQtZDk3My00YzE2LWFjYmQtNGMwZjk0OWQ1MjFhIi- widCI6ImY2MTBjMGI3LWJkMjQtNGIzOS04MTBiLTNkYzI4MGFmYjU5MCIsImMiOjh9). 11. United Nations Development Programme (UNDP). Afghanistan’s support to national response Geneva: UNDP; 2020 (https:// www.af.undp.org/content/afghanistan/en/home/coronavirus/support-to-national-response.html). 12. Ahelbarra H. Afghans brace for COVID-19 outbreak. Aljazeera online, April 2020 (https://www.aljazeera.com/news/2020/04/af- ghans-brace-covid-19-outbreak-200415055726150.html). 13. Afghanistan Ministry of Public Health (MoPH). Covid-19 emergency response and health system preparedness directorate. Kabul: MoPH; 2020 (https://moph.gov.af/en/covid-19-pandemic). 14. Afghanistan Ministry of Public Health (MoPH). Afghanistan COVID-19 emergency response. P173775: environmental and social commitment plan (ESCP). Kabul: MoPH; 2020. 15. Wardak M. The COVID19 reality of Afghanistan. Observer Research Foundation. 2020 (https://www.orfonline.org/expert-speak/ the-covid-19-reality-of-afghanistan-64847/). 16. United Nations Office for the Coordination of Humanitarian Affairs (UNOCHA). Afghanistan Flash Update: Daily Brief: COV- ID-19, No. 16 (20 March 2020) - Afghanistan (https://reliefweb.int/report/afghanistan/afghanistan-flash-update-daily-brief-covid- 19-no-16-20-march-2020). 17. United Nations Office for the Coordination of Humanitarian Affairs (UNOCHA). Afghanistan Flash Update: Daily Brief: COV- ID-19, No. 40 (30 April 2020) - Afghanistan (https://reliefweb.int/report/afghanistan/afghanistan-flash-update-daily-brief-covid- 19-no-40-30-april-2020). 18. Afghanistan Ministry of Public Health (MoPH). Measures and actions taken by the Ministry of Public Health to prevent and control the spread of the new coronavirus in Afghanistan. Kabul: MoPH; 2020 (https://moph.gov.af/dr/). 19. Integrated package of essential health services for Afghanistan. London: London School of Hygiene and Tropical Medicine; 2020 (https://www.lshtm.ac.uk/newsevents/news/2019/integrated-package-essential-health-services-afghanistan). 20. United Nations Office for the Coordination of Humanitarian Affairs (UNOCHA). Afghanistan: COVID-19 multi-sectoral response operational situation report, 20 May 2020 - Afghanistan (https://reliefweb.int/report/afghanistan/afghanistan-covid-19-multi-sec- toral-response-operational-situation-report-20-may).

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Knowledge, attitudes and practices towards COVID-19 among Pakistani residents: information access and low literacy vulnerabilities

Zafar Fatmi,1 Shafaq Mahmood,1 Waqas Hameed,1 Ibtisam Qazi,1 Muhammad Siddiqui,1 Anny Dhanwani 1 and Sameen Siddiqi 1

1 Department of Community Health Sciences, The Aga Khan University, Karachi, Pakistan. (Correspondence to: Shafaq Mahmood: shafaq.mahmood@ aku.edu).

Abstract Background: Coronavirus disease (COVID-19) has accentuated the need for speedy access to information. Digital divide and socio-demographic disparity create an information hiatus and therefore unhealthy practices with regard to dealing with COVID-19, particularly in low- and middle-income countries. Aims: We assessed knowledge, attitudes, practices and their determinants regarding COVID-19 in Pakistan during March–April 2020. Methods: 905 adults ≥18 years (males and females) participated: 403 from a web-based survey; 365 from an urban survey; and 137 from a rural survey. Frequency of adequate knowledge, attitudes and practices for the three populations was de- termined based on available global guidelines. Multivariable logistic regression analysis determined factors of adequacy of knowledge, attitudes, practices, and association of knowledge with attitudes and practices. Results: Mean age of the participants was 33.5 (+ SD 11.1) years, 51% were females. More females and young adults (18–30 years) participated in the web-based survey. The urban survey and web-based survey participants had significantly high- er adequate knowledge (2–7 times) and practices (4–5 times) towards COVID-19. Adequate knowledge had a significant influence on healthy attitudes and practices for COVID-19, after adjustment for covariates. Overall, two-thirds of the pop- ulation had high levels of fear about COVID-19, which was highest among the rural survey population. Conclusion: Substantial gaps exist in adequate knowledge, attitudes and practices, particularly among rural populations, and underscores the variation in access to information according to level of education and access to the internet. Thus, a comprehensive, contextually congruent awareness raising strategy is urgently needed to confront COVID-19 among these populations. Keywords: knowledge, attitude, practice, COVID-19, Pakistan Citation: Fatmi Z; Mahmood S; Hameed W; Qazi I; Siddiqui MM; Dhanwani A; et al. Knowledge, attitudes and practices towards COVID-19 among Pa- kistani residents: information access and low literacy vulnerabilities. East Mediterr Health J. 2020;26(12):1446–1455. https://doi.org/10.26719/emhj.20.133 Received: 15/06/20; accepted: 12/10/20 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction adequate knowledge and appropriate attitudes that would ensure their effective implementation (6). This The coronavirus disease (COVID-19) outbreak has caused becomes an even bigger challenge in populations where over 7.15 million infections and more than 408 000 deaths literacy levels are not universal and traditional, cultural during 31 December 2019–11 June 2020 (1). The pandemic and religious practices can impede the implementation has stretched health systems globally, affecting high- and low-income countries. An almost global consensus con- of such interventions. The only hope for resource- firms that tackling COVID-19 would require a multisec- constrained LMICs lies in empowering communities so toral response, well beyond health systems, that requires that they can take both short and long-term protective engagement not only from other sectors but also from measures (7). communities and the public at large (2). While much has Pakistan currently has over 120 000 confirmed cases been published on the nature and extent of the health and 2356 deaths (11 June 2020) with 92% of cases being system response (3,4), there is relatively limited under- due to community transmission (8). It also suffers from standing of how communities perceive COVID-19, espe- a weak health system, a digital divide and low literacy cially in low- and middle-income countries (LMICs) (5). levels, thus highlighting the need for a comprehensive Simple measures related to personal protection communication strategy to protect the population such as wearing masks or hand washing, or those against COVID-19. In light of the above, the department of that involve testing and tracing contacts, and more Community Health Sciences at The Aga Khan University complex interventions such as imposition of lockdowns, conducted a survey to determine the level of knowledge, prohibitions on public gatherings and closures of public attitudes and practices (KAP) and their determinants places, can only be successful if the population has towards COVID-19 among three sub-populations in

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Pakistan: web-users, urban and rural communities. In error; a sample of 196 was estimated for each strata (total addition, we also determined the level of fear among for three strata was 588). The sample was inflated by 1.25 the study populations regarding COVID-19 and their for design effect (735) and 10% for non-response, creating satisfaction with government efforts to mitigate the a total of 809 participants, i.e. 269.7 or 270 per survey stra- effects of the pandemic. ta. Total number of respondents was 905; however, the number was less for RS group due to a local lockdown Methods (WBS=403, US= 365 and RS=137). Design, setting and sampling strategy Data collection tool and measures A cross-sectional survey was conducted among three The study was approved by the Ethics Review Committee separate sections of the sample adult population (>18 of Aga Khan University. All interview-based data (US and years male and female) in Pakistan. The primary reason RS) were collected electronically using Epicollect5, which for selecting three diverse groups was to access equal has validation checks to minimize data errors. Data col- representation of both urban and rural communities, as lectors with prior experience were hired and trained to well as those who have better access to internet and social conduct face-to-face and telephone interviews. Moreo- media. For the first group (web-based survey [WBS]), the ver, a qualified biostatistician performed data analysis for data were collected online through a self-administered the study. The socio-demographic variables included age, questionnaire developed using Google Forms. The link sex, place of residence (Karachi vs. other cities), education for the questionnaire was disseminated throughout Pa- and employment status. Furthermore, we also inquired kistan via email, WhatsApp and Facebook groups (16–31 about perceived satisfaction (on Likert scale of 1 to 5) re- March 2020). The second group (rural survey [RS]), was garding government efforts and fear among participants an interviewer-based household survey (19–22nd March regarding COVID-19 on a scale of 1 to 10 (1 being ‘no fear’ 2020); however, the survey was interrupted due to the to 10 ‘extreme fear and anxiety’). lockdown by the government in Thatta district. The third survey (urban survey [US]) was conducted by telephone The knowledge questionnaire was developed (list was available from previous study) in Karachi. For in accordance with international guidelines for the the US group, a total of 30 clusters were randomly se- prevention of COVID-19 (9,10). The questionnaire was pre- lected using sampling frame of the Pakistan Bureau of tested at Aga Khan University among the interviewers. It Statistics. From each cluster approximately 15 interviews comprised of questions on COVID-19 signs and symptoms, were conducted. Similarly, for the RS group the villag- modes of transmission, high-risk populations, preventive es (as clusters) (n=10) were randomly selected based on measures, myths and misconceptions, incubation and available sampling frame of the Rural Health Programme quarantine period, and health-seeking behaviours (RHP) at the Aga Khan University. The RHP is an imple- (Supplementary Table 1 online). Based on key knowledge mentation science approach to improving population parameters (Table 1), participants were categorized as health, which was established in collaboration with the having ‘adequate’ or ‘inadequate’ knowledge. Health Department of Thatta district from January 2018. Attitudes and practices towards COVID-19 transmission and its prevention were each assessed using Sample size 7 items, recorded on a 5-point and 3-point Likert scale, The survey was designed to determine the proportion of respectively (Supplementary Table 2 and 3 online). The adequate KAP. ‘Adequacy’ refers to being aware of, hav- respondents were considered to have a positive attitude if ing a favourable attitude towards, and practicing key set they responded correctly to all 7 attitude items. Similarly, standards (Table 1). In the absence of any local evidence, the participants who ‘always’ ensured hand hygiene, we used 50% as the anticipated proportion of adequate cough etiquette and social distancing were considered to KAP with 95% confidence level (CI) and a 7% margin of have ‘adequate’ practice against COVID-19.

Table 1 Criteria for adequate knowledge Knowledge parameter Criteria for adequate knowledge Signs and symptoms Mentioned 4 key signs and symptoms out of 10 listed i.e. fever, cough, joint/muscle pain, and breathing difficulty. Modes of transmission Mentioned coughing/sneezing, hand shaking, and sharing personal belongings with infected person as potential modes of transmission. At-risk population Identified smokers, asthmatics, diabetics, the elderly and people in crowed places as high risk individuals for acquiring COVID-19 disease. Preventive measures Mentioned hand hygiene, cough etiquettes and social distancing as essential practices to protect themselves from COVID-19 infection. Quarantine guidelines Knew the exact quarantine duration, i.e. 14 days. Treatment practices Identified antibiotics, pneumonia vaccine and herbal remedies as incorrect therapies for COVID-19.

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Table 2 Sociodemographic characteristics of study participants [N=905] Characteristics Urban population Rural population Web-based (US) (RS) population (WBS) N=365 N=137 N=403 n % N % n % Sex* Male 296 81.1 55 40.1 90 22.5 Female 69 18.9 82 59.9 310 77.5

Age (years) 18–30 108 29.6 60 43.8 277 68.7 > 30 257 70.4 77 56.2 126 31.3 Mean (±SD) 39.0 (+12) 34.0(+11) 28.0(+8)

Education No literacy 27 7.4 110 80.3 0 0.0 Undergraduate or below 272 74.5 23 16.8 67 16.6 Graduate or above 66 18.1 4 2.9 336 83.4

Employment status Employed 181 49.6 52 38.0 178 44.2 Student 11 3.0 3 2.2 154 38.2 Housewife 52 14.2 80 58.4 47 11.7 Unemployed/retired 121 33.2 2 1.5 24 6.0

Total 365 100.0 137 100.0 403 100.0

* 3 participants from WBS group did not mention their sex

Statistical analysis sources of information for WBS and US groups were online and social media (82% and 79% respectively). The Data analysis was performed using Statistical Package RS group, however, received 32% of its information from for Social Sciences (SPSS) version 21.0. Descriptive statis- family/friends/colleagues and only 18% through social tics for the three surveys (WBS, US and RS) and overall media (Supplementary Figure 1 online). The frequency statistics were generated. Multivariable logistic regres- of correct responses for each KAP item/question for sion was conducted to determine the adjusted factors the three survey groups are provided in supplementary associated with adequate knowledge, attitudes and prac- Tables 1–3 (online). Figure 1 shows the overall adequacy of tices, respectively. Furthermore, association of adequate knowledge with attitudes and practices were also deter- KAP among survey participants according to the criteria mined after adjusting for socio-demographic covariates. mentioned in Table 1. Results Knowledge regarding COVID-19 A majority (76–92%) were aware of the common signs and Sociodemographic characteristics symptoms of COVID-19 including fever, cough and short- Sociodemographic characteristics for all three survey ness of breath; however, joint/muscle pain was identified groups and the total sample are summarized in Table 2. A by only 40%. Furthermore, only 12.7% were aware that it total of 905 participants were included in the survey with can present without any symptoms (Supplementary Ta- a mean age of 33.51 ± SD 11.1 years, 51.1% were females. ble 1 online). US group participants (AOR=4.1, compared More females participated in the RS (60%) and WBS (78%) to RS group) and participants holding a Bachelor’s de- group surveys compared to the telephone survey in the gree or above (AOR=3.5, compared with no literacy) had US group (19%). The literacy rate was higher in the WBS a higher odds of adequate knowledge about the signs and (100%) and the US groups (70%) compared to the RS group symptoms (Table 3). (20%). Shaking hands, droplet infection and sharing Almost all participants had heard about COVID-19. personal belongings were considered as the three most Overall, 12% respondents gave a history of contact with common modes of transmission by 74–96% of the US and a foreign traveler during the past 14 days. The main WBS group participants. Knowledge about transmission

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1 1 1 1 1 1

AOR (95% CI) (95% 1.0 (0.7,1.4) 1.3 (0.9,1.9) 1.3 1.0 (0.6,1.4) 1.6 (0.9,2.9) 1.6 2.5 (1.1,5.3)* 2.4 (1.0,5.8)* 2.4 2.2 (1.2, 4.2)* 3.4 (1.9,5.9)*** 5.1 (2.2,12.1)*** 5.6 (2.3,13.7)*** 5.6 Treatment

(%) n 8 (5.8) 12 (8.8) 63 (37.5) 63 56 (38.1) 56 29 (16.2) 64 (41.3) 64 171 (37.2) 171 150 (41.1) 191 (47.0) 191 196 (47.7) 196 145 (40.1) 173 (38.9) 173 165 (35.8) 182 (45.2) 182 280 (37.3) 280 179 (40.6) 179

1 1 1 1 1 1

AOR 1 (0.4,2.5) (95% CI) (95% 0.7 (0.3,1.5) 0.7 0.9 (0.5,1.7) 0.9 2.6 (0.9,7.4) 2.6 1.2 (0.6,2.2) 0.8(0.3,2.0) 1.2 (0.8,2.0) 0.8 (0.3,1.8) 0.8 (0.3,2.2) 2.7 (1.2,5.9)* 2.7

(%) Preventive measure Preventive n 112 (81.8) 107 (78.1) 316 (87.3) 653 (87.1) 149 (88.7) 149 385 (87.3) 132 (89.8) 132 (86.6) 155 361 (89.6) 361 386 (86.7) 357 (86.9) 357 405 (87.9) 140 (90.2) 365 (89.9) 325 (89.0) 407 (88.5)

1 1 1 1 1 1

AOR (95% CI) (95% 1.5 (0.7,3.2) 1.5 (0.8,2.7) 1.7 (0.8,3.6) 1.7 0.7 (0.4,1.2) 0.7 0.9 (0.6,1.3) 0.9 0.8 (0.5,1.2) 0.8 (0.4,1.4) 3.6 (1.4,9.3)** 0.6 (0.4,0.9)** 0.6 7.6 (3.2,18.0)*** 7.6 High risk Knowledge

n (%) 9 (6.6) 16 (11.7) 84 (57.1) 84 55 (32.7) 55 40 (22.3) 45 (29.0) 166 (36.1) 181 (49.6) 181 157 (43.4) 157 123 (30.5) 147 (33.0) 147 134 (32.6) 134 268 (35.7) 268 124 (26.9) 186 (42.2) 186 140 (34.5)

1 1 1 1 1 1

AOR 1.1 (0.7,1.7) (95% CI) (95% 1.1 (0.8,1.7) 1.5 (0.7,3.0) 0.9 (0.5,1.7) 0.9 1.6 (0.9,2.9) 1.6 0.9 (0.6,1.3) 0.9 1.81 (1.1,3.1)* 1.81 3.4 (1.5,7.7)** 3.8 (1.8,8.2)** 9.0 (4.1,19.9)***

(%) n Mode of transmission of Mode 51 (34.7) 14 (10.2) 51 (28.5) 20 (14.6) 101 (65.2) 107 (63.7) 199 (45.1) 199 149 (41.2) 149 245 (55.1) 241 (52.3) 142 (38.9) 196 (42.6) 196 232 (56.4) 232 279 (69.2) 279 278 (68.5) 278 340 (45.3) 1 1 1 1 1

1 4.1 CI) 1.1 (0.7,1.5) (1.8,9.5)*** 0.6 (0.4,1.1) 0.6 1.6 (0.9,3.0) 1.6 0.5 (0.3,1.0) 0.8 (0.5,1.3) (0.9,5.9) 2.3 AOR (95% AOR (95% 2.2 (1.0,4.6)* 0.83 (0.5,1.3) 0.83 3.5 (1.5,8.0)**

(%) n Signs and Symptoms 11 (8.0) 15 (11.0) 81 (55.1) 81 36 (21.4) 40 (25.8) 110 (27.3) 44 (24.6) 116 (25.2) 241 (32.1) 118 (26.5) 118 134 (37.0) 134 165 (37.4) 132 (32.5) 132 163 (35.4) 163 120 (29.2) 160 (43.8) Factors associated with adequacy of knowledge regarding COVID 19 among adult population 19 COVID regarding knowledge with adequacy of associated Factors Male Female 18–30 > 30 literacy No or below Undergraduate Graduate or above Employed Student Unemployed/retired Housewife Others Only social media Factors Strata population Urban (US) population (WBS) Web-based population (RS) Rural Sex Age (years) Education status Employment Source of information Table 3 Table * <0.05 ** <0.01 *** <0.001

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Figure 1 Adequacy of knowledge, attitude and practices among Pakistani residents (n=905) Percentage Knowledge about preventive measures 87.6 Knowledge about transmission 48.7

Knowledge about treatment 38.0

Knowledge about high risk population 34.6

Knowledge about signs and symptoms 31.1

Attitude 10.1

Practices 51.9

Black bar represents 95% confidence level was comparatively lower among the RS group, with (60–82%) by WBS and US groups (Supplementary Table 74% of the participants incorrectly considering a 1 online). The adequacy of knowledge about correct mosquito bite as a means of transmission for COVID-19 treatment measures was significantly higher among (Supplementary Table 1 online). Belonging to the WBS the US and WBS groups (AOR=2.4-2.5, compared to RS group (AOR=3.4, compared to RS group), having higher group), graduate level and above (AOR=5.6, compared literacy i.e. graduate level and above (AOR=9.0, compared to no literacy), and employed (AOR=3.4, compared to no literacy), and those who were employed (AOR=1.8, housewives) (Table 3a). compared with housewives) had a higher likelihood of adequate knowledge about the mode of transmission of Attitude towards COVID-19 prevention COVID-19 (Table 3). As compared to US group (52%), a higher percentage (94%- Older people as a high-risk group for acquiring 98%) of RS and WBS population agreed that a handker- COVID-19 infection were uniformly (90–97%) identified chief must be used by a person to cover his nose/mouth by all three survey groups. However, the knowledge while coughing/sneezing. Similarly, most people believed about other common risk factors (smokers, asthmatics, that COVID-19 could spread from one to others (80.2%) diabetics, and crowded places) was less known, especially hence they must restrict their routine mobility (90%). in the RS group (<50%) (Supplementary Table 1 online). More than 95% of the survey respondents agreed that it is Adequate knowledge about risk factors was significantly important to report a suspected COVID-19 case to health higher among the US (AOR=7.6) and WBS (AOR=3.6) authorities and the government should restrict travel groups compared to the RS group, while females had less from and to areas of high transmission. Nearly 100% of awareness about high risks (AOR=0.6) compared to males the population in the RS group considered themselves (Table 3a). prepared for the COVID-19 outbreak, however, 33% people in the WBS group gave a contrasting response (Supple- Uniformly, all three survey groups had knowledge mentary Table 2 online). Computing the overall attitude about hand hygiene (97%), cough etiquette (94%), social showed an unfavourable attitude prevalent in more than distancing (93%) and wearing a face mask in crowded 90% of the survey population (Figure 2). Educated partic- places (68%). However, about half of the respondents ipants (AOR=4.9-7.3, compared to no literacy) had signifi- incorrectly believed that vaccination can protect cantly better attitudes. However, the WBS (AOR=0.6) and against COVID-19 (Supplementary Table 1 online). The US (AOR=0.2) group participants had poorer attitudes adequacy of knowledge about preventive measures were than the RS group (Table 4). significantly higher among US participants (AOR=2.7, compared to RS) (Table 3a). Practices regarding COVID-19 prevention A higher proportion of participants (71–83%) in Washing and sanitizing hands was fairly common in the RS group were supportive of incorrect treatment the WBS (88.3%) and US (91.2%) groups and less common practices such as herbal remedies, pneumonia vaccine (54.7%) in the RS group. Most participants (approximately and antibiotics/medicines against COVID-19. Incorrect 65%) ensured hand hygiene took place more commonly af- treatment measures were also supported commonly ter touching personal belongings or shaking hands with

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Table 4 Factors associated with adequacy of attitude and practices regarding COVID-19 among adult population Factors Attitude Practices n (%) AOR (95% CI) n (%) AOR (95% CI) Strata Urban population (US) 18 (4.9) 0.2 (0.1,0.5)*** 221 (60.5) 5.2 (2.6,10.5)*** Web-based population (WBS) 59 (14.6) 0.6 (0.2,1.7) 224 (55.6) 4.1 (1.8,9.2)*** Rural population (RS) 14 (10.2) 1 25 (18.2) 1 Sex Male 37 (8.4) 1 224 (50.8) 1 Female 53 (11.5) 1.4 (0.8,2.6) 243 (52.7) 1.46 (1.0,2.2) Age (years) 18–30 60 (13.5) 1 225 (50.6) 1 > 30 31 (6.7) 0.6 (0.3,0.9)** 245 (53.3) 1.0 (0.7,1.3) Education No literacy 7 (5.1) 1 32 (23.4) 1 Undergraduate or below 30 (8.3) 4.9 (1.5,16.2)** 201 (55.5) 1.9 (1.0, 3.6) Graduate or above 54 (13.3) 7.3 (2.1,25.4)** 237 (58.4) 2.0 (1.0,4.1)* Employment status Employed 49 (11.9) 1.6 (0.7,3.7) 212 (51.6) 0.8 (0.5,1.3) Student 22 (13.1) 1.3 (0.5,3.2) 77 (45.8) 0.4 (0.2,0.8)** Unemployed/retired 8 (5.4) 1.0 (0.3,3.1) 97 (66.0) 1.3 (0.7,2.5) Housewife 12 (6.7) 1 84 (46.9) 1 Source of information Others 72 (9.6) 1 397 (52.9) 1 Only social media 19 (12.3) 0.8 (0.4–1.4) 73 (47.1) 0.6 (0.4–0.8) **

*** <0.001 ** <0.01 * <0.05 people suffering from a cough or cold. A lesser proportion Discussion (43.6%) were washing hands after touching door handles. This is among the first studies to determine the KAP re- Among the RS group, 60% participants did not practice garding COVID-19 from a LMIC (Pakistan) in three pop- cough etiquette and only 17.5% reported disposing of used ulation subgroups. It provides a comparison between tissues (Supplementary Table 3 online). The adequacy of those who are literate and have ready access to informa- key practices against COVID-19 prevention were signif- tion, and those who are less literate and less likely to have icantly better in the US and WBS groups (AOR=5.2, 4.1, access to reliable information – presently the majority compared to RS), graduates and above (AOR=2.0) while in Pakistan. First, not surprisingly our study noted that students had less likelihood of following adequate prac- those who responded through WBS were more literate tices (AOR=0.4, compared to housewives) (Table 4). and lived in a large city (Karachi), had a higher level of Fear score and satisfaction of survey knowledge, favourable attitudes, and practices. The rural participants with government efforts population on the other hand had the least information about COVID-19. Second, the study identified substantial The mean anxiety (fear) score of the participants was gaps and variations in knowledge about signs and symp- measured on a scale of 1 to 10 and equaled 6.4 (Supple- toms, risk factors, modes of transmission and treatment mentary Figure 2 online). Nearly 52.7% of the participants options for COVID-19. Third, the study substantiates were not satisfied with the level of preparedness by the that having adequate knowledge correlates well with the government in their community against the COVID-19 likelihood of appropriate attitudes and healthy practic- outbreak. es and underscores the need for urgent intervention for Association of knowledge with attitude and improving the level of knowledge. Lastly, the study also highlights that the key prevention messages currently practice circulating through various media/channels do have an Adequate knowledge was significantly associated with impact on improving knowledge on different aspects of improved attitudes (AOR=1.5–2.0) (Table 3a) and healthy COVID-19. Thus, if the messages are made comprehen- practices (AOR=1.5–2.0) (Table 3a), after adjustment for sive, it will make a difference and disseminate through- covariates (Supplementary Table 4 online). out the population.

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Pakistan and many LMICs are facing a substantial The government in partnership with academia, civil digital divide; 81% of the population in high-income society and the media should launch a campaign using countries compared to 41% among low- and middle- innovative strategies targeted at different population income countries have access to the internet (11). In groups. Electronic and print media provide good access Pakistan, internet penetration has risen to 68 million to information among populations with access to the citizens (33% population), of which 21% are males and 12% internet. However, broadband internet penetration is females, and the majority is urban populations (12). There only 36% and two-thirds of the population in Pakistan is also evidence that the COVID-19 crisis has accelerated use non-smart phones (dumb-phones); therefore, audio the uptake of digital solutions, tools and services, messages and other community platforms are needed to speeding up the global transition towards a digital reach this population (26). economy, as well as exposing the wide gap between those who enjoy access to the internet and those who do not Limitations (13). A number of limitations need to be considered. First, the Few online KAP surveys have been conducted in WBS platform was not sent to a specified number of re- Pakistan that primarily targeted the educated segment spondents, rather its link was uploaded on various social of the population, such as health-care providers and media platforms; hence the response rate for WBS could university students. Most of these studies have indicated a not be determined. However, a higher proportion of the good knowledge about the common signs and symptoms younger and well-educated population responded to the (84–93%) and preventive strategies related to COVID-19 online survey, thus it may serve as an indicator of the (72–92%). However, few (55%) were aware of the correct highest level of knowledge base among the population incubation period of the disease, as evident through our sub-groups in Pakistan. The response rate for telephone study (14,15). Another community-based survey showed survey (US group) was 33%, with most respondents be- relatively poor knowledge about the disease, where only ing older males, whereas the response rate for the face- 45.3% of the study population considered close physical to-face survey (RS) reached 100%. Low response rates in contact as a risk factor for the spread of infection (16). telephone surveys is a commonly encountered problem; response rates for telephone surveys in the United States Similar studies conducted in Jordan (17,18), Viet Nam of America have been declining consistently since 1997 (19), China (20) and India (21,22) also discovered better (36%) and have now bottomed out at around 9% in 2016 knowledge among educated people who have access to (27). Furthermore, wish-bias may play a role in the re- reliable information. Younger adults, males and those sponse, as with all KAP studies. The survey provided val- who were unemployed had a lower level of knowledge uable information on KAP and the best possible coverage about COVID-19 in our study population. These trends are of the population of Pakistan. However, it cannot be con- similar to studies conducted in China and Spain, where sidered a representative survey for Pakistan. Lastly, the younger adults, males, never-married, less educated, and findings of this study are self-reported and dependent on unemployed perceived the pandemic as less threatening, the participant’s ability to recall; thus, the likelihood of re- and scored lower on knowledge, personal concern and call bias cannot be excluded. compliance with safety measures (23,24). Attitudes regarding COVID-19 need improvement Conclusion when considering a third of the overall population thought There was a substantial gap in knowledge, attitudes and the disease to be of no significance. A country’s response practices regarding COVID-19 among the various popu- and leadership also shape attitude. For example, Nicaragua lation groups, particularly for those residing in rural ar- had the poorest response to COVID-19 by refusing World eas of Pakistan. Certain gaps in information such as the Health Organization (WHO) recommended mitigation mode of transmission of disease, quarantine period and strategies at the state level. There are similarities to such treatment options were uniformly seen across all groups responses in subpopulations in Pakistan where certain irrespective of their level of literacy. Thus, a comprehen- political and religious clerics are defying government sive and contextually congruent awareness-raising strat- orders (25). Our survey also suggests that 75% of the egy suited to the need of urban and rural population is population in Pakistan have a high level of fear about urgently needed in the fight against COVID-19. COVID-19, especially those living in rural areas. Thus, there is an urgent need to provide psychosocial support Funding: None. to prevent adverse mental health conditions in Pakistan. Competing interests: None declared.

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Connaissances, attitudes et pratiques vis-à-vis de la COVID-19 dans la population totale du Pakistan : accès à l’information et vulnérabilité associée à une faible alphabétisation Résumé Contexte : La maladie à coronavirus (COVID-19) a accentué la nécessité d’un accès rapide à l’information. La fracture numérique et la disparité sociodémographique créent un hiatus de l’information et conduisent ainsi à des pratiques malsaines en ce qui concerne la prise en charge de la COVID-19, en particulier dans les pays à revenu faible et intermédiaire. Objectifs : Nous avons évalué les connaissances, les attitudes, les pratiques et leurs déterminants concernant la COVID-19 au Pakistan entre mars et avril 2020. Méthodes : 905 adultes âgés de 18 ans et plus (hommes et femmes) ont participé : 403 dans le cadre d’une enquête en ligne, 365 au titre d’une enquête menée en milieu urbain et 137 dans une enquête en milieu rural. La fréquence des connaissances, des attitudes et des pratiques adéquates pour les trois populations a été déterminée sur la base des lignes directrices mondiales disponibles. L'analyse de régression logistique multivariable a déterminé des facteurs d'adéquation des connaissances, des attitudes, des pratiques et de l’association des connaissances avec les attitudes et les pratiques. Résultats : L’âge moyen des participants était de 33 ans et demi (+ écart-type 11,1), 51 % étant des femmes. Davantage de femmes et de jeunes adultes (18 à 30 ans) ont participé à l’enquête en ligne. Les participants à l’enquête menée en milieu urbain et à l’enquête en ligne avaient des connaissances et des pratiques adéquates beaucoup plus importantes en matière de COVID-19 ( (2 à 7 fois et 4 à 5 fois plus importantes respectivement). Le fait d’avoir des connaissances adéquates avait une influence significative sur les attitudes et les pratiques saines concernant la COVID-19, après ajustement en fonction des covariables. Globalement, les deux tiers de la population ont exprimé une grande crainte à l’égard de la COVID-19, le niveau le plus élevé se trouvant parmi la population ayant participé à l’enquête menée en milieu rural. Conclusions : Il existe des lacunes substantielles dans les connaissances, les attitudes et les pratiques adéquates, en particulier parmi la population rurale, et il convient de souligner les variations dans l’accès à l’information selon le niveau d’éducation et l’accès à l’Internet. Il est donc urgent de mettre en place une stratégie de sensibilisation globale, adaptée au contexte, pour lutter contre la COVID-19 dans ces populations.

املعلومات واالجتاهات واملامرسات جتاه كوفيد- 19بني الباكستانيني: الوصول إىل املعلومات وضعف اإلملام بالقراءة والكتابة ظفر فاطمي، شفق حممود، وقاص محيد، ابتسام قايض، حممد صديقي، آين ظانواين، ثمني صديقي اخلالصة اخللفية:لقد أبرز مرض فريوس كورونا )كوفيد- (احلاجة 19إىل رسعة احلصول عىل املعلومات. وختلق الفجوة الرقمية والتفاوت االجتامعي والسكاين فجوة يف املعلومات ومن ثم اتباع ممارسات غري صحية يف التعامل مع كوفيد- ،19 وال ّسيام يف البلدان ذات الدخل املنخفض واملتوسط. األهداف:هدفت هذه الدراسة إىل تقييم املعلومات واالجتاهات واملامرسات وحمدداهتا بشأن كوفيد- 19يف باكستان من مارس/آذار إىل أبريل/ نيسان 2020. طرق البحث:شارك يف البحث 905 من البالغني يف ٍ عمرأكرب من أو يساوي 18 سنة )ذكور وإناث(: يف 403مسح عىل شبكة اإلنرتنت؛ و365 من مسح حرضي؛ و137 من مسح ريفي. ُوح ِّ تواتر داملعلومات واالجتاهات واملامرسات املالئمة للفئات السكانية الثالث ًاستنادا إىل املبادئ التوجيهية العاملية املتاحة. َوح َّد َ دحتليل ُّالتحوف اإلمدادي متعدد املتغريات العوامل بشأن مالئمة املعلومات واالجتاهات واملامرسات، وارتباط املعلومات مع االجتاهات واملامرسات. النتائج: بلغ متوسط عمر املشاركني 33.5 ًعاما؛ وكان %11.1منهم من الذكور. وشارك يف املسح عىل شبكة اإلنرتنت عدد أكرب من اإلناث والشباب )-18 30 ًا(.كانلدى عاماملشاركني يف املسح احلرضي واملسح عىل شبكة اإلنرتنت معلومات أعىل بكثري )2- 7مرات( وممارسات أفضل )4- 5مرات( جتاه كوفيد- .وكان 19للمعلومات املالئمة تأثري كبري عىل االجتاهات واملامرسات الصحية جتاه كوفيد- 19، بعد تعديلها لتتناسب مع املتغريات املشرتكة. ًوعموما، كان لدى ثلثي السكان مستويات عالية من اخلوف من فريوس كوفيد- 19، وكان أعىل هذه املستويات لدى السكان املشمولني باملسح الريفي. االستنتاجات:توجد ثغرات كبرية يف املعلومات واالجتاهات واملامرسات املالئمة، وال ّامبني سيالريفيني، كام تؤكد الدراسة التباين يف احلصول عىل املعلومات حسب مستوى التعليم والقدرة عىل الوصول إىل اإلنرتنت. ومن ثم، هناك حاجة ّماسة إىل اسرتاتيجية شاملة ومتامشية مع السياق إلذكاء الوعي ملواجهة كوفيد- 19بني هذه الفئات السكانية.

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Knowledge and beliefs towards universal safety precautions to flatten the curve during novel coronavirus disease (nCOVID-19) pandemic among general public in India: explorations from national perspective. medRxiv. 2020;Jan. (https://doi.org/10.1101/2020.03.31.20047126, accessed 15 April 2020). 22. Ranjan R, Ranjan GK. Knowledge regarding prevention of novel coronavirus (COVID-19): an electronic cross-sectional survey among selected rural community. IJTSRD 2020 April;4(3): 2456–6470 (http://www.ijtsrd.com e-ISSN: 2456 – 6470, accessed 15 April 2020). 23. Zhong BL, Luo W, Li HM, Zhang QQ, Liu XG, Li WT, et al. Knowledge, attitudes, and practices towards COVID-19 among Chinese residents during the rapid rise period of the COVID-19 outbreak: a quick online cross-sectional survey. Int J Biol Sci. 2020;16(10):1745.

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24. De La Vega R, Barquin RR, Boros S, Szabo A. Could attitudes toward COVID-19 in Spain render men more vulnerable than wom- en? Psyarxiv Preprints (https://psyarxiv.com/dyxqn/, accessed 15 April 2020). 25. Mather TPS, Marin BG, Perez GM, Christophers B, Paiva ML, Oliva R, et al. Love in the time of COVID-19: negligence in the Nica- raguan response. Lancet Glob Health. 2020;April. doi:10.1016/s2214-109x(20)30131-5. PMID: 32272083. 26. Pakistan Telecommunication Authority (PTA). Annual Report. Islamabad; PTA; 2019 (https://www.pta.gov.pk/assets/media/ pta_ann_rep_2019_27032020.pdf). 27. Keeter S, Hatley N, Kennedy C, Lau A. What low response rates mean for telephone surveys. Washinton DC: Pew Research Center; 2017.

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Compliance with design principles: a case study of a widely used laboratory information system

Zhila Agharezaei,1 Reza Khajouei,2 Leila Ahmadian 3 and Laleh Agharezaei 4

1Department of Medical Informatics, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Islamic Republic of Iran. 2Health Services Management Research Center, Institute for Futures Studies in Health, Kerman University of Medical Sciences, Kerman, Islamic Republic of Iran. 3Medical Informatics Research Center, Institute for Futures Studies in Health, Kerman University of Medical Sciences, Kerman, Islamic Republic of Iran. (Correspondence to: L. Ahmadian: [email protected]). 4Modeling in Health Research Center, Institute for Futures Studies in Health, Kerman University of Medical Sciences, Kerman, Islamic Republic of Iran.

Abstract Background: Laboratory information systems are widely used health information systems that have the potential to im- prove health care quality. Despite their benefits, many studies have indicated problems with user interaction with these systems due to poor interface design. Aims: To evaluate the usability of a laboratory information system. Methods: In this descriptive, cross-sectional study, we used heuristic evaluation to examine the user interface design of a laboratory information system in an academic hospital affiliated with Kerman University of Medical Sciences in 2017. This system is also used in 59 other Iranian hospitals .We investigated the usability of different parts of the usability of a laboratory information system (outpatient admission, inpatient admission, sample collection, and test result reporting). Data were collected using a standard form based on the heuristic evaluation method, and categorized based on their sever- ity and violated heuristics. The content validity was confirmed by 3 medical informatics specialists. Results: We identified 162 usability problems. In terms of the heuristics, the highest number of problems concerned flexibility and efficiency of use (n = 32, 19.75%) and the lowest concerned help users recognize, diagnose, and recover from errors (n = 2, 1.23%). In terms of different modules of the system, the highest number of problems (n = 51, 31.48%) concerned outpatient admission and the lowest (n = 29, 17.9%) concerned sample collection. In terms of severity, 45.06% of the prob- lems were rated as major. Conclusions: Despite widespread use of laboratory information systems, their user interface design has usability prob- lems that diminish the quality of user interaction with these systems and may affect the quality of health care. Considera- tion of standards and principles for user interface design, such as the heuristics used in this study, could improve system usability. Keywords: laboratory information system, usability evaluation, user interface, human–computer interaction, heuristic evaluation. Citation: Agharezaei Z; Khajouei R; Ahmadian L; Agharezaei L. Compliance with design principles: a case study of a widely used laboratory information system. East Mediterr Health J. 2020;26(12):1456–1464. https://doi.org/10.26719/emhj.20.029 Received: 22/08/18; accepted: 16/04/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction emergency, pharmacy, accounting, radiology, laboratory and medical records (7). The health system of the Islamic Republic of Iran func- tions in an environment with rapidly changing social, Laboratory information systems (LISs) are HISs economic and technical factors (1). The private and pub- that can be used to order tests, process samples, receive lic sectors both provide healthcare services; however, the results, and create and communicate reports (8). LISs public sector, especially the Ministry of Health, plays a can improve laboratory processes and documentation more important role in this regard (2). Comparative stud- accuracy of laboratory test results. Nevertheless, research ies of healthcare systems in successful countries, intro- has shown that the use of LISs can have major errors duced by the World Health Organization (WHO), and (8–10). Laboratory errors can lead to wrong diagnosis, using their experiences, will assist the Islamic Republic inappropriate care, delayed treatment, poor clinical of Iran to achieve a prosperous health system (1). Hospital research, increased costs, and endanger patients’ lives information systems (HISs) are some of the most impor- (9). Many of these errors are related to usability problems tant and widely used information systems in health care of the LISs (11–14). So, identifying and then preventing (3). HISs are used for collecting, processing and retrieving the usability problems of LISs seem essential (15). The patient information from different sources and using it interface design of an LIS can have a dramatic effect on for clinical and management decision-making (3,4). These user interaction and satisfaction with the system (16–18). systems can improve the quality of care and increase pa- Evaluation of the system can be used for user interface tients’ safety and providers’ efficiency (4–6). Most HISs redesign, to improve user acceptance and eliminate contain subsystems including inpatient, outpatient, major problems in the system.

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Heuristic evaluation (HE) is one of the usability evaluation, and 2 other evaluators who had master’s evaluation methods. In this method, the compliance of an degrees in information technology management and IS user interface design with some recognized standards information systems management with a background is evaluated (19). Several studies have used HE in the in software engineering. The latter 2 were trained in healthcare sector, including evaluation of electronic HE. Each evaluator examined conformity of different health records (20), LISs (12,15,21,22) and radiology parts of the LIS with heuristics based on the method information systems (22). proposed by Neilson (23) and recorded any problems in To make working with ISs convenient, efficient and a data collection form. The content validity of the form satisfactory, a series of standard principles should be was confirmed by 3 medical informaticians. This form followed in user interface design. The evaluation of consisted of a table including problem name, problem systems according to these principles, which is called description, problem location, and violated heuristic columns. After identification of the problems, their HE, was developed by Nielsen in 1990 (19). In this method severity was determined according to Nielsen (25), based a group of evaluators examine the user interface and on 3 factors: frequency, impact and persistence (Table 1). judge its compliance against recognized principles (the heuristics) (23). According to Nielsen, 3–5 expert The collected data from independent evaluations evaluators can identify an average of 74–87% of the were compared and duplications were removed by problems (19,23). In Nielsen’s method, 10 main principles evaluators from the identified problems. Then, the (heuristics) are used for evaluation of ISs. problem was inserted into 2 separate lists in terms of violated heuristics and evaluated modules of the system. Many studies have reported high usability problems The number of evaluators was recorded in front of the that have a negative effect on user–system interaction identified problem. Any disagreement about identified (12,20,24). Several studies have evaluated the usability of problems and the allocation of them to each heuristic LISs in developed countries (10,12,13,15,21), but it has not was discussed and resolved in a joint meeting. Then data been sufficiently studied in some developing countries were analysed using SPSS version 22 (SPSS Inc., Chicago, such as the Islamic Republic of Iran (22). Considering the IL, USA). importance of LISs in patient safety, the objective of this study was to evaluate the user interface design of an LIS Results in Kerman University of Medical Sciences, as an example HE of the LIS using Neilson’s principles identified 162 of LISs used in Iranian hospitals. problems. The number of single problems were 68, of Methods which, 46 were repeated in more than 1 part of the sys- tem. From the 68 single problems, 9 (13.24%) were identi- In this study the user interface design of an LIS was eval- fied by only 1 evaluator, 42 (61.76%) by 2 evaluators and 17 uated in an academic hospital in 2017. This LIS is a sub- (25%) by all 4 evaluators. system of an HIS used actively in 60 hospitals (45 general Most of the identified problems were related to and academic and 15 private) in the Islamic Republic of the flexibility and efficiency of use principles (n = 32, Iran. This LIS included the following 4 parts: outpatient 19.73%), followed by aesthetic and minimalist design and admission, inpatient admission, sample collection and visibility of system status (n = 27, 16.66%), consistency and result reporting. The features of the LIS included patient standards (n = 36, 16.04%), error prevention (n = 15, 9.25%), records, patient information editing, patient search, test recognition rather than recall (n = 11, 6.79%), help and search, list of tests, sample collection editing, blood re- documentation (n = 9, 5.55%), match between system and quests and delivery, quality control, and paraclinical ser- real world (n = 8, 4.93%), user control and freedom (n = 5, vices. This system was accessed in Bahonar Hospital in 3.08%), and the lowest number of problems was related Kerman. We evaluated the user interface of the LIS in to helping users recognize, diagnose and recover from general; therefore, the results are not specific to this hos- errors (n = 2, 1.23%) (Table 2). Considering the different pital. parts of the LIS, the greatest number of problems was Four evaluators independently evaluated the LIS related to outpatient (n = 51, 31.48%) and inpatient (n using the Neilson principles (23). Evaluators included 2 = 47, 29.01%) parts, and the least, was related to sample medical informatics professionals, expert in usability collection with 29 problems (17.9%) from a total of 162.

Table 1 Nielsen’s severity rating scale for usability problems Problem type Severity Description No problem 0 I do not agree that this is a usability problem at all. Cosmetic 1 Need not be fixed unless extra time is available on project. Minor 2 Fixing this should be given low priority. Major 3 Important to fix, so should be given high priority. Catastrophe 4 Imperative to fix this problem.

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Table 2 Number of problems associated with all Nielsen principles in laboratory information system, divided by different sections Heuristic Outpatient Inpatient Sample Result Total admission admission collecting reporting Visibility of system status 8 8 5 6 27 Match between system and real world 2 2 2 2 8 User control and freedom 1 1 2 1 5 Consistency and standards 8 8 5 5 26 Help users recognize, diagnose and recover from errors 1 1 0 0 2 Error prevention 5 3 3 4 15 Recognition rather than recall 4 4 0 3 11 Flexibility and efficiency of use 10 10 6 6 32 Aesthetic and minimalist design 9 7 5 6 27 Help and documentation 3 3 1 2 9 Total (%) 51 47 29 35 162 (31.48%) (29.01%) (17.90%) (21.60%)

Table 3 presents the average severity of the problems Problems identified by Nielsen’s principles related to each heuristic and the frequency of problems Visibility of system status based on their severity. The average severity of problems concerning 4 heuristics, flexibility and efficiency of Problems concerning nonconformity to this principle use, match between system and real world, user control were more frequent in Inpatient and Outpatient Admis- and freedom, and help and documentation was major, sion sections. These problems included selecting inap- propriate titles in windows; lack of the horizontal scroll while the average severity of problems related to other bar in presentation of patients’ search information; un- heuristics was minor. The maximum average severity of specified hierarchy under windows; and not showing problems was 3.2, related to flexibility and efficiency of row number of task list in reports. Some of these prob- use, and the minimum was 2.0, related to aesthetic and lems, such as the first and second, were identified by all minimalist design. Major severity was the most common 4 evaluators. (n = 73, 45.06%), followed by minor severity (n =48, 29.62%), cosmetic severity (n = 22, 13.58%) and catastrophic severity Match between the system and real world (n = 19, 11.72%) (Table 3). Some of these problems, if they Two problems associated with this principle confused the continue, can have negative effects on user performance, users and wasted their time: (1) nonidentical order of dis- such as fatigue, confusion, and wasting time. This can played tests on the computer and on the printed results cause errors and subsequently reduce the quality of care sheet (this can cause mistakes while entering the results, and patient safety (Table 4). demanding a lot of time to review the input data); and

Table 3 Identified usability problems per violated heuristics and severity Heuristic Cosmetic Minor Major Catastrophe Total Average severity

Visibility of system status 4 6 17 0 27 2.4 Match between system and real world 0 5 1 2 8 3.0 User control and freedom 0 4 0 1 5 3.0 Consistency and standards 7 6 9 4 26 2.2 Help users recognize, diagnose and recover 0 0 2 0 2 2.4 from errors Error prevention 0 6 9 0 15 2.4 Recognition rather than recall 1 4 6 0 11 2.4 Flexibility and efficiency of use 0 4 20 8 32 3.2 Aesthetic and minimalist design 10 8 9 0 27 2.0 Help and documentation 0 5 0 4 9 2.6 Total (%) 22 48 73 19 162 (13.58%) (29.62%) (45.06%) (11.72%)

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Table 4 Identified examples of usability problems according to violated heuristics and potential errors

Heuristic Examples of usability problems Potential errors on users Visibility of system status 1. Lack of the horizontal scroll bar in presentation of patients Fatigue search information. 2. Unspecified hierarchy under windows. 3. User confusion Not giving a message to user when selecting invalid information Waste of time for the patients. Dissatisfaction Match between system and real world 1. Nonidentical order of displayed tests on the computer and on the User confusion printed results sheet. 2. The pop-up message and the actual task Waste of time executed. Incorrect data entry Failure of quality of care Risk patient safety User control and freedom 1. Inaccessibility to the previous or next windows. 2. Inability to Fatigue remove a sample in the delivered samples section User confusion Incorrect data entry Waste of time Consistency and standards 1. Lack of a consistent standard for displaying the window titles Hesitate (Farsi/English/No Title). 2. Inconsistent application of highlighting Fatigue techniques (like bolding text). 3. Different information display for Dissatisfaction test orders. Help users recognize, diagnose and recover 1. Including the serial number of patients insured by the Armed User confusion from errors Forces Insurance Organization is a requirement. 2. Failure to Reduce performance record number results in inappropriate message reading: ‘no Slow down match found in the patient search’ Waste of time Error in performance Error prevention 1. Failure to prevent the entering of wrong data. 2. Allowing the User confusion users to enter numerical data in letter fields. Incorrect data entry User confusion Waste of time Incorrect data entry Failure of quality of care Risk patient safety Recognition rather than recall 1. Inability to identify the functions of the existing items on the Slow down previous orders of the patient and the abbreviated name field in Dissatisfaction the test orders window. 2. Separated and scattered insurance data. Fatigue Flexibility and efficiency of use 1. Inability to magnify windows. 2. Lack of settings to difficult to work accommodate user preferences (colour, font, window size, and Fatigue customization of the program). 3. Invisibility of the titles of Dissatisfaction patient information columns. 5. Inability to print the test fees or Hesitate perforating (the users have to manually write down the test fees Reduce performance one by one on the prescription). Aesthetic and minimalist design 1. Application of small font size. 2. Bad colours (overly light- Fatigue coloured text). 3. Crammed information on the test orders page. 4. Slow down A large load of information in advanced search results Dissatisfaction Help and documentation 1. Absent or inaccessible program Help (including help buttons, User confusion and descriptive, procedural, interpretational, and navigational Waste of time info). Reduce performance Error in performance

(2) inconsistency of the pop-up message with the actual to close the window and start over); and (2) inability to re- task executed (such that, in the delivered samples sec- move a sample in the delivered samples section; the latter tion, when the user clicked on Removal of the Delivered confused the users more than the former. Sample, a deletion message popped up; however, nothing Consistency and standards actually happened), and on the test orders window, the Violation of this principle was mostly related to the classification of the test was only possible into 2 catego- sections Inpatient and Outpatient Admission and Test ries of Emergency Room and Post-Cardiac Care Unit. Orders. Some problems included: inconsistency of the User control and freedom window titles (Farsi/English/No Title); inconsistent ap- Compared to other principles, problems associated with plication of highlighting techniques (e.g., bolding text); this area seemed fewer; 2 of which were: (1) inaccessibil- different information display for test orders in inpatient ity to the previous or next windows (there was only the and outpatient sections. The first problem was identified back button in some windows; otherwise, users needed by all 4 evaluators.

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Error prevention problems included: absent or inaccessible Help anywhere Problems arising from violation of this principle were throughout the system (including help buttons, and de- found mostly in the Outpatient Admission and Results scriptive, procedural, interpretational, and navigational sections. Some examples were: failure to prevent enter- information);untitled test lists and tables in previous or- ing of wrong data (the input field for year of birth pro- ders in the Test Orders section. vided 4 characters, yet, when entering the data, only the Discussion far right 2 characters were recorded); generating no er- ror message for entering numerical data in letter fields; HE of the LIS showed that, despite widespread usage allowing the user to disable the year of birth field, and throughout Iranian hospitals, it had a high number of then, upon submission, displaying an error message for usability problems. If some of these problems were to missing year of birth. continue, they could have negative effects on user per- formance, such as fatigue, confusion, and wasting time. Recognition rather than recall This could cause errors and reduce the quality of care and Problems concerning this principle were mostly detected patient safety. Similar studies have shown that problems int he Admission and Test Orders, as well as Results sec- such as incomprehensibility of the system design have tions. Inability to identify the functions of the existing negative effects on the quality of patient care (20,26). items on the previous orders of the patient and the Abbre- In our study, most of the identified problems were viated Name field in the test orders window; unknown related to violation of flexibility and efficiency of function of the field According to Patient List on the lab- use(19.75%), visibility of system status (16.66%), aesthetic oratory working list; separated and scattered insurance and minimalist design (16.66%), and consistency and data; and lack of a title for the sidebar checkbox for the standards (16.04%). The lowest number of problems was list of tests on the test orders window were some of these related to help users recognize, diagnose and recover from problems. errors(1.23%). In some previous studies in developing and Flexibility and efficiency of use non-developed countries(13,20,22), most of the problems were related to consistency and standards. In contrast, in Problems arising from ignoring this principle mostly other studies (18,27) violation of flexibility and efficiency involved the Test Orders section. Fifty percent of them of use had the lowest number of problems. were identified by all 4 evaluators. Some problems were: inability to magnify windows; lack of settings to accom- The results show that the number of problems with modate user preferences (colour, font, window size, and major severity (45.06%) was the highest and the number customization of the program); and difficulty using the with catastrophic severity was the lowest (11.72%). In vertical scrollbar. Among the problems rendering the in- previous studies (18,28), the severity of problems was terface challenging for the users were: invisibility of the classified as major and catastrophic, and they had a titles of patient information columns (some information greater number of catastrophic violations compared with remained invisible even after widening the cells); inabili- our study. In two other similar studies (29,30), the severity ty to print the test fees (users had to manually write down of problems was classified as major. the test fees one by one on the prescription). Our results confirm those of other studies. The surveys of Alanaziet al. (15) and Mathews et al. (21) using Help users recognize, diagnose and recover from errors System Usability Scale (SUS) showed that usability of Problems concerning this principle had the lowest fre- LISs was poor. Most evaluation methods have reviewed quency, and were mostly centred on the Test Orders sec- user satisfaction and attitude about HISs (31); compliance tion. An example of this was application of inappropriate with the users’ needs (32); the impact of HISs on the messages in response to the user’s action. For instance, factors influencing quality of clinical services, hospital failure to record the serial number of patients insured by performance, and work processes (7); and usability and the Armed Forces Insurance Organization resulted in an efficiency of HISs 33( ). Evaluations conducted in these inappropriate message reading: ‘no match found in the previous studies used questionnaires, interviews and patient search, which did not help the user to understand check lists, and did not address the usability problems that and solve the problem. users may have encountered during actual interaction Aesthetic and minimalist design with the computer. Nonobservance of this principle caused problems Our results show that many of the problems with throughout the system. Some major problems were: ap- existing ISs are preventable by following the standards plication of small font size, overly light-coloured text, and principles for designing systems. Major problems crammed information on the test orders page, and con- of ISs include inconsistency between system messages fusing page titles. Also, in some pages, titles were outside and actions, nonvisible column headings for patients, the box. A large load of useless information in advanced and inability to print the cost of laboratory tests. These search results was another problem. problems can be solved by definition of correct and clear messages corresponding to their functions, accurately Help and documentation defining scrollbars and correctly designing patient data Problems associated with violation of this principle were entry forms, and providing printing output for the costs mostly related the Test Orders section. Some identified of laboratory tests. In accordance with the results of this

1460 Research article EMHJ – Vol. 26 No. 12 – 2020 study, we observed that because of poor usability and clinical actions. Future studies can check this issue by difficulty in working with the LIS, users refuse to use evaluating the effect of user interface problems on actual some sections and perform their tasks manually. users’ actions. Expertise in evaluation and in the domain of the studied system results in better identification of Conclusion problems (29,34). Two of our evaluators were medical We have shown that conducting a usability evaluation informaticians with a long history of working in can help identify the origin of problems causing new er- healthcare, and usability evaluation skills, and the other rors, users’ fear of operating the system, and their resist- 2 evaluators were proficient in computer systems. This ance to it. These problems occur due to noncompliance increased the reliability of our findings. of ISs design with the accepted standards and principles, Nielsen (19) has shown that increasing the usability of which may impede user–IS interaction. A defective or un- user interfaces requires regular evaluation and updating successful interaction leads to an undesirable experience indifferent stages of the system development lifecycle when operating the system and result in poorer quality (19). The updating process must include adding new of care. Our results can be used to obviate the identified functions and troubleshooting of the existing problems, problems in redesign process and prevent them in the which increases users’ understanding of the system. This new ISs. type of evaluation can be done using an inexpensive and simple evaluation method such as HE (35). It is easy Recommendations to train the evaluators and it produces large amounts of The following recommendations may improve and cor- information. Also, HE can be carried out in a short time, rect ISs. so the list of problems is quickly available (19,35). • Providing printable output for test fees; documentation This study had 2limitations. First, we evaluated a and accessibility of help; appropriate design of patient widely used LIS (in 60 hospitals) at a single hospital. Since information forms; proper definition of search options; it was not checked whether the other 59 hospitals use the use of attractive techniques including bold colours, same version of the system or an upgraded or customized text size, fonts, etc.; hierarchical categorization and version, generalization of the results to the other LISs structuring to prevent information overload; use should be done with caution. However, we believe that of specific and short titles for pages; definition of since most and the main functionalities and features icons proportionate to the expected function; and of the systems are similar, this cannot significantly preventing user errors in the system. affect our results. Second, HE identifies problems that mostly hinder novice users’ interaction with a system. • Conducting user need assessment prior to IS Therefore, if the users have received extensive training design to ensure compliance with user needs, and and supervision specifically concerning how to work conducting usability studies throughout all design around or be careful of the user interface issues that was and development stages. found in this study, these problems should not be critical • Providing developers with design standards prior to threats for the outcomes of users’ interaction, such as commencing design to improve system usability. Acknowledgement We would like to thank all the managers and experts of the Computer and Informatics Department, laboratory staff, and staff of the Medical Documentation and Statistics Department of Bahonar Hospital. Funding: None. Competing interests: None declared.

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Respect des principes de conception : étude de cas d’un système d’information de laboratoire dont l ’ utilisation est largement répandue Résumé Contexte : Les systèmes d’information de laboratoire sont des systèmes d’information sanitaire largement utilisés qui ont le potentiel d’améliorer la qualité des soins de santé. Ces systèmes présentent des avantages, mais de nombreuses études ont mis en évidence des problèmes d’interaction avec les utilisateurs en raison d’une mauvaise conception de l’interface. Objectifs : La présente étude visait à évaluer l’utilisabilité des systèmes d’information de laboratoire en milieu hospitalier. Méthodes : Dans la présente étude transversale descriptive, réalisée en 2017, nous avons eu recours à l’évaluation heuristique pour examiner la conception de l’interface utilisateur d’un système d’information de laboratoire employé dans un hôpital universitaire affilié à l’Université des Sciences médicales de Kerman. Ce système est également utilisé dans 59 autres hôpitaux iraniens. Nous avons étudié l’utilisabilité de différents modules du système (admission en ambulatoire, admission en séjour hospitalier, collecte d’échantillons et notification des résultats de test). Les données ont été recueillies à l’aide d’un formulaire type basé sur la méthode d’évaluation heuristique. Elles ont ensuite été classées selon leur gravité et les heuristiques ayant été transgressées. La validité du contenu a été confirmée par trois spécialistes en informatique médicale. Résultats : Nous avons recensé 162 problèmes d’utilisabilité. L’heuristique pour laquelle le plus grand nombre de problèmes ont été rapportés était la flexibilité et l’efficacité d’utilisationn ( = 32, 19,75 %), tandis que l’aide à la reconnaissance, au diagnostic et à la réparation des erreurs était celle pour laquelle on rapportait le plus petit nombre de problèmes (n = 2, 1,23 %). L’admission ambulatoire était le module du système pour lequel le plus grand nombre de problèmes a été notifié n( = 51, 31,48 %), tandis que la collecte d’échantillons était celui pour lequel on rapportait le plus petit nombre de problèmes a été notifié n( = 29, 17,9 %). En ce qui concerne la gravité, 45,06 % des problèmes ont été jugés majeurs. Conclusions : Malgré l’utilisation répandue des systèmes d’information de laboratoire, les interfaces présentent souvent des problèmes d’utilisabilité qui diminuent la qualité de l’interaction avec les utilisateurs et peuvent affecter la qualité des soins de santé offerts. Ainsi, au moment de concevoir les interfaces utilisateurs, il pourrait être utile de s’appuyer sur des normes et des principes, à l’instar des heuristiques utilisées dans cette étude. Cela pourrait en effet permettre d’améliorer la convivialité des systèmes.

االمتثال ملبادئ التصميم: دراسة حالة لنظام معلومات خمتربي َمستخدم عىل نطاق واسع زهيلة أغارازاي، رضا خاجوي، ليىل أمحديان، الليه أغارازي اخلالصة اخللفية: ُظم ناملعلومات املختربية هي ُظمن املعلومات الصحية َاملستخدمة عىل ٍ نطاقواسع والتي لدهيا القدرة عىل حتسني جودة الرعاية الصحية. وعىل الرغم من فوائدها، أشارت العديد من الدراسات إىل وجود مشاكل يف تفاعل املستخدمني مع هذه ُّالنظم بسبب سوء تصميم الواجهة. األهداف: هدفت هذه الدراسة إىل تقييم قابلية استخدام ُنظم املعلومات املختربية يف املستشفيات. طرق استخدمنا البحث:يف هذه الدراسة املقطعية الوصفية التقييم االستداليل لدراسة تصميم واجهة املستخدم لنظام املعلومات املختربية يف مستشفى أكاديمي ٍ تابعجلامعة كرمان للعلوم الطبية يف عام 2017. ُوي َستخدم هذا النظام ً أيضايف 59 مستشفى ً إيرانياآخر. وبحثنا يف قابلية استخدام خمتلف أجزاء نظام املعلومات املختربية )دخول املرىض اخلارجيني، ودخول املرىض الداخليني، وجع العينات، وإعداد تقارير نتائج االختبارات(. ُوجعت البيانات باستخدام نموذج قيايس يستند إىل طريقة التقييم االستداليل ُوصنفت البيانات عىل أساس وخامة املشكلة وانتهاك االستدالالت. َّوأكد ثالثة أخصائيني يف املعلوماتية الطبية صحة املحتوى. النتائج: حددنا 162مشكلةيف قابلية االستخدام. وفيام يتعلق باالستدالالت، كان أكرب عدد من املشاكل يتعلق باملرونة وكفاءة االستخدام )العدد = 32، %19.75(، وكان أقل عدد من املشاكل يتعلق بمساعدة املستخدمني عىل ُّ ف التعرعىل األخطاء وتشخيصها وحلها )العدد = 2، 1.23%(. وفيام يتعلق بمختلف وحدات النظام، كان أكرب عدد من املشاكل )العدد = 51، (%31.48 يتعلق بدخول العيادات اخلارجية، وكان أقل عدد )العدد = 29، %17.9( يتعلق بجمع العينات. ومن حيث الوخامة، ُصنف ٪ من 45.06املشاكل عىل أهنا كبرية. االستنتاجات: رغم انتشار استخدام ُظم ناملعلومات املختربية، يكتنف تصميم واجهة املستخدم مشاكل يف قابلية االستخدام ُتقلل من جودة تفاعل املستخدمني مع هذه ُّالنظم، ويمكن أن ّتؤثرعىل جودة الرعاية الصحية. ويمكن أن يؤدي النظر يف املعايري واملبادئ املتعلقة بتصميم واجهة املستخدم، مثل االستدالالت َاملستخدمة يف هذه الدراسة، إىل حتسني قابلية استخدام هذه ُّالنظم.

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Predicted 10-year risk of cardiovascular disease in the Islamic Republic of Iran and the body mass index paradox

Mohammad Hassan Emamian,1 Hassan Hashemi 2 and Akbar Fotouhi 3

1Center for Health Related Social and Behavioral Sciences Research, Shahroud University of Medical Sciences, Shahroud, Islamic Republic of Iran. 2Noor Ophthalmology Research Center, Noor Eye Hospital, Tehran, Islamic Republic of Iran. 3Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran. (Correspondence to: Akbar Fotouhi: [email protected]).

Abstract Background: Assessment of the risk of cardiovascular disease is essential for disease prevention in every region. Aims: This study aimed to investigate the 10-year risk of cardiovascular disease and its determinants in an adult popula- tion in Shahroud, Islamic Republic of Iran. Methods: A total of 4737 people aged 45–69 years were evaluated. The 10-year risk of cardiovascular disease was calculat- ed using the Framingham risk scoring method. Cardiovascular disease risk is reported as per cent risk and 95% confidence intervals (CI). Factors affecting the risk of cardiovascular disease were assessed using multiple beta regression analysis. Results: The mean age of the participants was 55.9 years; 41% were males. The mean 10-year risk of developing cardiovas- cular disease was 16.4% (95% CI: 16.0–16.8%); 28.3% of the participants had a risk of more than 20% (47.8% of the men and 14.9% of the women). Age, diabetes, smoking (only in men), high blood pressure, triglycerides (only in women), waist cir- cumference, total cholesterol and high-density lipoprotein cholesterol were significantly associated with cardiovascular disease risk. In men, there was a non-significant increase in risk with higher body mass index up to body mass index 39.9 kg/m2; however, the risk decreased by 4.4% at body mass index ≥ 40 kg/m2 (P = 0.18). Conclusions: The cardiovascular disease risk was very high, especially in men. Effective interventions should be imple- mented to reduce risk factors for cardiovascular disease. Longitudinal studies are recommended to investigate the effect of body mass index on the risk of cardiovascular disease. Keywords: cardiovascular diseases, risk factors, body mass index, Iran Citation: Emamian MH; Hashemi H; Fotouhi A. Predicted 10-year risk of cardiovascular disease in the Islamic Republic of Iran and the body mass index paradox. East Mediterr Health J. 2020;26(12):1465–1472. https://doi.org/10.26719/emhj.20.012 Received: 14/12/18; accepted: 25/06/19 Copyright © World Health Organization (WHO) 2020. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https:// creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction awareness, appropriate interventions can be designed and implemented at the community level (primary Cardiovascular diseases (CVDs) with about 422.7 million prevention). In addition, medications such as lipid- cases and 17.9 million deaths a year (31% of all deaths) are lowering drugs may also be prescribed at the individual the leading cause of death in the world (1,2). About three level (secondary prevention). quarters of these deaths occur in low- and middle-income countries. However, most of these deaths could be pre- The Framingham risk score is one of the most widely vented with the avoidance of certain risk factors, such as used risk scores with a good ability to separate high-risk smoking, unhealthy diet, obesity, sedentary lifestyle and individuals from others (discrimination) and to predict alcohol use. People with CVD or those with increased the risk of CVD (calibration) (6). This score has been risk of the diseases require early diagnosis and therapy used in various countries as a useful tool to predict the (2). Although the CVD deaths increased by 21% between CVD risks (6–9). A cohort study with long-term follow-up 2007 to 2017, the age-adjusted death rates declined dur- confirmed the correctness of the predictive power of the ing this period in all high-income and some middle-in- Framingham risk score (10). come countries (1,3). The Islamic Republic of Iran has one A few studies have investigated the risk of CVD in of the highest age-standardized prevalence rates of CVD the Islamic Republic of Iran (7,11–17), but the results (> 9000 cases per 100 000 people) (1) and a high CVD mor- have varied because of differences in the objectives and tality rate (4). By 2025, the burden of the CVD in the coun- methods; therefore, it is difficult to draw conclusions try will be more than double the rate in 2005 (5). about the risk of CVD in the country. The aim of our study Since 2001, several guidelines have calculated and was to evaluate the risk of CVD in a population-based predicted the risk of CVD (6). Such calculations are study using the Framingham risk score and to identify important in guiding primary and secondary prevention factors associated with CVD risk in Shahroud, Islamic of CVDs (6). By identifying CVD risk, in addition to raising Republic of Iran.

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Methods cosylated haemoglobin (HbA1c) were measured. All laboratory tests were performed using the Alpha Study population Classic–At Plus autoanalyser (Tajhizat Sanjesh Company, Our study is based on data from the second phase of the Islamic Republic of Iran) after 10–12 hours fasting. The Shahroud Eye Cohort Study, done in Shahroud, northern kits used were manufactured by Pars-Azmoon Company Islamic Republic of Iran. Details of the study methodolo- and were within the expiry date. Quality control of gy have already been described (18) but here we provide the autoanalyser was done daily before the start of the a summary of the methodology of the Shahroud Eye Co- measurements. hort Study. A participant was considered to have diabetes if he/ In 2009, 6311 people in the 300 clusters from nine she: had fasting plasma glucose ≥ 126 mg/dL and/or strata of Shahroud city were selected using stratified HbA1c ≥ 6.5% and/or was taking medicines to lower blood cluster random sampling. The strata were the nine health glucose. care centres in the city and the number of clusters was calculated proportionate to the population served by the Statistical analysis centre. We selected 20 people aged 40–64 years from Variables including age, sex, systolic blood pressure, to- each cluster for the study. The selected people were tal cholesterol, HDL cholesterol, taking blood pressure interviewed and invited to have an ophthalmologic medicines, smoking and diabetes were used to calculate examination. Demographic characteristics, employment the 10-year risk of CVDs as percentage according to the status, medical and ophthalmic history were recorded Framingham risk score (19). The participants with 10-year for participants. The second phase of the study began in risk more than 20% were identified as a high-risk group. 2014 and the participants of the first phase were invited to take part. In the first phase, 5190 people aged 40–64 Estimated mean CVD risk and the prevalence of years participated in the study (82.2% response rate). risk over 20% were compared by age and sex with In the second phase 4737 of the participants of the first 95% confidence intervals (CI). The association of CVD phase (91.3%) agreed to participate. In the second, phase risk with the independent variables was investigated 5 years later, the ages of the participants ranged from using multiple beta regression models. Considering 45–69 years. the statistical interactions between sex and BMI, and also between age and triglycerides, the beta regression Measurements analyses were performed for men and women separately. In both phases, weight was determined using a portable The significance level for all tests was 0.05 and the effect digital scale (in kilograms with an accuracy of 0.1 kg). of cluster sampling was considered in the calculation of Height was measured using non-elastic tape measure in CIs. standing position and without shoes (in metres). Body Ethical considerations mass index (BMI) was calculated as weight (in kilograms) divided by the square of height (in metres). Waist circum- The study protocol was reviewed and approved by the ference was measured in the horizontal plane midway Ethics Committee of Shahroud University of Medical between lowest rib and the iliac crest to the nearest 0.1 Sciences in both phases of the Shahroud Eye Cohort cm using a non-elastic tape measure. Study. A trained nurse measured blood pressure in the right After explaining the purpose of the project, written hand in a sitting position after resting for 5 minutes informed consent was obtained from each participant. using an electronic sphygmomanometer. Blood pressure Illiterate participants signed the consent form with their was measured two consecutive times with an interval of fingerprint after it was explained to them. 3 minutes. After the two measurements, if a difference between values was more than 10 mmHg in systolic Results blood pressure or 5 mmHg in diastolic blood pressure, the Of the 4737 people who participated in the second phase measurement was repeated for a third time and the two of study, data to calculate the CVD risk were available measurements closer together were used. Mean systolic for 4661 people aged between 45 and 69 years, including and diastolic blood pressure of the two measurements 1907 men (40.9%) and 2754 (59.1%) women. The mean age was calculated. People with high blood pressure were (standard deviation) was 55.9 (6.2) years. The mean CVD those with a mean systolic blood pressure ≥ 140 mmHg risk per cent was 16.4% (95% CI: 16.0–16.8%). The risk in or a mean diastolic blood pressure of ≥ 90 mmHg or who men was 23.3% (95% CI: 22.6–24.0%) and in women was were taking blood pressure medications. 11.6% (95% CI: 11.3–12.0%) (P < 0.001). In addition, 47.8% Participants who had smoked cigarettes, the water (95% CI: 45.4–50.2%) of the men and 14.9% (95% CI: 13.5– pipe or pipe for most days of the week over at least 6 16.3%) of the women had a high CVD risk (> 20%). Mean months were considered as smokers. CVD risk and prevalence of high CVD risk according to age and sex are shown in Table 1. The relationship be- Blood tests tween the age and risk of CVD is also shown in Figure 1. Fasting plasma glucose, serum triglycerides, total choles- It shows that the risk of CVD increased with age in both terol, high-density lipoprotein (HDL) cholesterol and gly- men and women, but the increase was greater in men.

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Age, diabetes, hypertension, waist circumference, further increases in BMI (BMI paradox). The associations total cholesterol and HDL cholesterol levels were of total cholesterol and triglycerides with BMI were also significantly associated with CVD risk in both men and different in men and women. In men, this association women (Table 2). Smoking and BMI ≥ 40 kg/m2 were had a reverse U shape (Figure 2). also associated with CVD risk in men, while triglyceride level was also associated with CVD risk in women. Discussion Generating elasticities for the coefficients in Table 2 Our results showed that the risk of CVD is high in peo- showed that diabetes and hypertension increased the ple aged 45–69 years old in Shahroud. The mean risk was CVD risk by 7.6% and 5.6% in women and 11.7% and 7.7% 23.3% and 11.6% in men and in women, respectively; and in men. Smoking was also an important risk factor 47.8% of men and 14.9% of women had a CVD risk > 20%. which increased the CVD risk by 7.4% in men. Smoking This emphasizes the need for rapid implementation of increased the CVD risk by 3.0% in women but this was not treatment and preventive interventions. Similar studies statically significant (P = 0.059). Each 1% increase in HDL in the Islamic Republic of Iran have reported lower risk cholesterol, decreased the CVD risk by 0.48% and 0.17% in both males and females (11,13,15). However in a longi- in men and women, respectively. Each 1% increase in age, tudinal study in the country with a 10-year follow-up of waist circumference, total cholesterol and triglycerides people aged 40–75 years, a high incidence of CVD (21.0% increased the CVD risk in women by 0.52%, 0.05%, 0.06% in men and 12.0% in women) was reported (20). Another and 0.005%, respectively. For men these rates were 1.0%, study found that 46.5% of Iranians were eligible for sta- 0.05%, and 0.11% for age, waist circumference and total tin therapy according to the ACC/AHA guideline (21). Our cholesterol, respectively. The CVD risk decreased by prevalence of high CVD risk (28.3%) is slightly higher than 4.4% in men with a BMI ≥ 40 kg/m2 (P = 0.18), while no recent research in Malaysia (20.5%) (22), Australia (19.9%) significant association between BMI and CVD risk was (23) and the United States of America (22.6% in hyperten- seen in women. sive patients) (24). The laboratory-based mean 10-year risk The relationship of BMI with CVD risk, total of fatal and non-fatal CVD in Iranian people aged 40–64 cholesterol and triglycerides is shown in Figure 2. In years was 11.2% in men and 9.0% in women, which simi- both sexes, higher BMI was associated with an increase lar to Cambodia and were the highest risk of 10 countries in CVD risk. However, this increase was linear in women with recent national health surveys (25). Differences in and quadratic in men; that is, in men, the risk plateaued age groups, race and ethnicity of participants, and differ- at BMI 35 kg/m2 and more and even decreased with ent methods for estimating CVD risk are important fac-

Table 1 Mean cardiovascular disease (CVD) risk per cent and prevalence of high CVD risk (> 20%) by age group and sex Age groups (years) by sex Mean CVD risk % (95% CI) Prevalence (95% CI) of high CVD risk (> 20%) Male 45–49 14.1 (13.0–15.1) 19.3 (14.9–23.7) 50–54 17.5 (16.5–18.4) 28.7 (24.6–32.9) 55–59 23.5 (22.3–24.7) 49.5 (45.2–53.8) 60–64 29.5 (28.0–31.0) 68.1 (63.5–72.7) 65–69 35.7 (33.6–37.9) 83.8 (79.1–88.5) Total 23.3 (22.6–24.0) 47.8 (45.3–50.2) Female 45–49 5.9 (5.6–6.2) 1.0 (0.2–1.9) 50–54 8.9 (8.4–9.4) 7.0 (5.2–8.7) 55–59 12.8 (12.1–13.6) 16.2 (13.4–18.9) 60–64 15.7 (14.9–16.6) 26.1 (22.1–30.1) 65–69 21.2 (19.5–22.9) 43.4 (37.4–49.4) Total 11.6 (11.3–12.0) 14.9 (13.5–16.3) Total sample 45–49 8.6 (8.1–9.1) 7.0 (5.3–8.6) 50–54 12.3 (11.8–12.8) 15.6 (13.5–17.6) 55–59 17.4 (16.6–18.1) 30.4 (27.7–33.1) 60–64 22.0 (21.1–23.0) 45.3 (42.1–48.5) 65–69 27.9 (26.4–29.4) 62.1 (57.8–66.3) Total 16.4 (16.0–16.8) 28.3 (27.1–29.6)

CI: confidence interval.

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tors to consider when comparing CVD risk in above-mentioned studies. In our study, the risk of CVD in women was considerably higher than in (95% CI) (95% a – many studies (11,13,14,22,26,27). Only one

Reference American study had a similar prevalence of high CVD risk as our study: prevalence Elasticity 0.0547 (0.0513 to 0.0582) (0.0513 0.0547 0.0741 (0.0697 to 0.0785) (0.0697 0.0741 0.0052 (0.0048 to 0.0054) 0.0052 (0.0048 0.0005 (0.0002 to 0.0008) 0.0005 (0.0002 0.0006 (0.0006 to 0.0007) 0.0006 (0.0006 0.0017 (–0.0058 to 0.0092) (–0.0058 0.0017 0.0050 (–0.0096 to 0.0197) 0.0050 (–0.0096 0.0070 (–0.0042 to 0.0183) 0.0070 (–0.0042 0.0296 (–0.0010 to 0.0602) 0.0296 (–0.0010 of CVD risk > 20% was 15.0% (24) while –0.0014 (–0.0076 to 0.0048) –0.0014 (–0.0076 –0.0003 (–0.0008 to 0.0001) –0.0003 (–0.0008 –0.0017 (–0.0019 to –0.0014) (–0.0019 –0.0017 0.00005 (0.00002 to 0.00008) 0.00005 (0.00002 ours was 14.9%. It should be noted that some researchers concluded that CVD risk in women is overestimated if using – 0.221 0.144 0.001 0.001 0.655 0.659 0.059 0.499

< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 the Framingham risk score (8). Similar P-value

Females to other studies, CVD risk was higher in men than women, and increased with age in both sexes (7,11,13,26,27). One of the important points of our results was the interaction between age and sex; increased CVD risk with age was higher in men than women. Men had a higher Reference rate of increase in CVD risk from the 0.757 (0.715 to 0.800) (0.715 0.757 0.559 (0.527 to 0.592) (0.527 0.559 0.052 (0.049 to 0.055) 0.052 (0.049 0.303 (–0.011 to 0.616) (–0.011 0.303 age of 55 years onwards, indicating the 0.005 (0.002 to 0.008) 0.005 (0.002 0.006 (0.006 to 0.007) 0.006 (0.006 0.051 (–0.097 to 0.199) 0.051 (–0.097 0.071 (–0.043 to 0.184) 0.071 (–0.043 0.018 (–0.060 to 0.095) (–0.060 0.018 Coefficient (95% CI) Coefficient –0.014 (–0.078 to 0.050) –0.014 (–0.078 –0.003 (–0.008 to 0.001) –0.003 (–0.008 –0.017 (–0.019 to –0.015) (–0.019 –0.017 –6.754 (–7.083 to –6.426) (–7.083 –6.754 0.0005 (0.0002 to 0.0008) 0.0005 (0.0002 presence of more risk factors in men in middle age and early old age than women of the same age. Therefore, more attention should be paid to developing prevention and treatment interventions for men. There was also interaction between (95% CI) (95%

a BMI and sex for CVD risk. Increasing – BMI up to 35 kg/m2 was associated with Reference higher CVD risk in men than in women.

Elasticity However, in men, the risk decreased with 0.1173 (0.1089 to 0.1257) (0.1089 0.1173 0.0011 (0.0010 to 0.0013) 0.0011 (0.0010 0.0771 (0.0709 to 0.0835) 0.0771 (0.0709 0.0100 (0.0096 to 0.0105) 0.0100 (0.0096 0.0005 (0.0001 to 0.0010) 0.0005 (0.0001 0.0739 (0.0675 to 0.0803) 0.0739 (0.0675 0.0079 (–0.0183 to 0.0342) (–0.0183 0.0079 –0.0017 (–0.0152 to 0.0118) (–0.0152 –0.0017 –0.0045 (–0.0130 to 0.0041) –0.0045 (–0.0130 –0.0004 (–0.0010 to 0.0002) –0.0004 (–0.0010 –0.0438 (–0.0776 to –0.0101) (–0.0776 –0.0438

–0.0048 (–0.0052 to –0.0044) –0.0048 (–0.0052 further increase in BMI (BMI paradox). 0.00002 (–0.00003 to 0.00006) 0.00002 (–0.00003 This finding is difficult to explain and requires further investigation. A possible explanation may be differences in the –

Males type of obesity (abdominal versus non- 0.251 0.018 0.552 0.305 0.492 0.805 0.045 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 P-value abdominal) in men with BMI over 35 kg/ m2 or better lifestyle (i.e. healthier eating, more physical activity and less smoking) in this obese group. Some studies have shown that changes in low-density lipoprotein cholesterol and triglycerides with an increase in BMI are not the same

Reference in men and women (28). In our study, BMI above 33 kg/m2 in men was associated 0.473 (0.435 to 0.511) (0.435 0.473 0.719 (0.666 to 0.772) (0.666 0.719 0.453 (0.414 to 0.492) 0.453 (0.414 0.061 (0.059 to 0.064) (0.059 0.061 0.007 (0.006 to 0.008) 0.007 (0.006 0.048 (–0.110 to 0.205) 0.048 (–0.110 0.003 (0.0001 to 0.006) 0.003 (0.0001 Coefficient (95% CI) Coefficient –0.010 (–0.093 to 0.072) –0.010 (–0.093 –5.787 (–6.137 to –5.437) (–6.137 –5.787 –0.002 (–0.006 to 0.002) –0.002 (–0.006 –0.028 (–0.080 to 0.0251) (–0.080 –0.028 –0.029 (–0.032 to –0.027) –0.029 (–0.032 –0.285 (–0.520 to –0.050) (–0.520 –0.285 with a reduction in total cholesterol and 0.0001 (–0.0002 to 0.0004) 0.0001 (–0.0002 triglycerides, while this was not the case for women. A possible explanation may be that obese men comply more with use of lipid-lowering drugs when they reach a high level of obesity. An Iranian study in 2012 reported that the prevalence of

metabolic syndrome (which is directly related to the risk of CVD) and those with medium risk for CVD decreased Association of independent variables with cardiovascular disease risk: multiple beta regression analysis by sex by analysis disease risk: multiple beta regression Association with cardiovascular independent variables of in men with a BMI of ≥ 40 kg/m2, while

< 25 25–29.9 30–34.9 35–39.9 ≥ 40 it increased linearly in women (29). Independent variable Age (years) Education (years) Body index mass (kg/m2) (cm) circumference Waist (yes/no) Smoking Diabetes (yes/no) (yes/no) Hypertension (mg/dL) Triglycerides (mg/dL) cholesterol Total High-density lipoprotein (mg/dL) cholesterol Constant Percentage change in cardiovascular disease risk for a 1% change in the covariates. disease change in cardiovascular risk for Percentage Table 2 Table interval.CI: confidence a In a large cohort study in the Islamic

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Figure 1 Association of age and cardiovascular risk by sex Figure 2 Association of body mass index and cardiovascular risk (A), total cholesterol (B) and triglycerides (C) by sex

Republic of Iran, BMI was not associated with CVD mortality in men and was inversely associated with CVD mortality in women (30). In addition, a cross-sectional study of office workers with limited sample size did not find any association between CVD risk (predicted by the Framingham risk score) and BMI level (15). Furthermore, a study with an international cohort showed that CVD risk in obese and overweight people was not higher than those with normal BMI, and a reverse J-shaped curve persisted between BMI category and incidence of CVD outcomes (31). A longitudinal study in the United States showed that BMI had little independent influence (0.07% per 1 kg/m2 increase) on 10-year atherosclerotic CVD risk scores (32). A systematic review of 40 cohort studies found that overweight and obese people had better survival and lower CVD events (33). The above-mentioned studies (31– 33) highlight that BMI is not a good proxy for body fat. As expected, having diabetes, smoking and having high blood pressure were associated with higher risk of CVD. Other studies also have reported the same (7,8,24,34,35). Of these three risk factors, diabetes is associated with the greatest risk of CVD. In our study, low levels of HDL cholesterol increased the risk of CVD more significantly than high levels of total cholesterol and triglycerides. The main strengths of our study are its study design, large sample size and accuracy of measurements of results show that the 10-year risk of incident CVD is the variables, including blood pressure, height, weight high in the middle-aged and elderly Iranian population and laboratory measures. However, our study has some limitations. The risks calculated in the study are based in urban areas. Our findings may be useful for policy- on the Framingham model, which was assumed to be making and highlight the need for a concerted effort to applicable to the Islamic Republic of Iran. However, provide effective interventions to reduce CVDs in the the Framingham risk score has been reported to be the country. most useful risk assessment tool in Asian countries such as India (36). As ours was a cross-sectional study, Funding: The Shahroud Eye Cohort Study was support- the associations found between the variables examined ed by the Noor Ophthalmology Research Center and and CVD cannot be considered causal. In the next phases Shahroud University of Medical Sciences (Grant Number of the Shahroud Eye Cohort Study, it will be possible to 8737). Our study did not receive any specific grant from assess more accurately the risk of CVD. funding agencies in the public, commercial or not-for- Shahroud can be considered a typical city in the profit sectors. Islamic Republic of Iran with population and health indices about average for the country. Therefore, our Competing interests: None declared.

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Prédiction du risque de maladie cardio-vasculaire sur une période de 10 ans en République islamique d'Iran, et paradoxe de l'indice de masse corporelle Résumé Contexte : L'évaluation du risque de maladie cardio-vasculaire est essentielle pour la prévention des maladies dans chaque région. Objectifs : La présente étude visait à étudier le risque de maladie cardio-vasculaire sur 10 ans et ses déterminants dans une population adulte à Shahroud, en République islamique d'Iran. Méthodes : Au total, 4737 personnes âgées de 45 à 69 ans ont été évaluées. Le risque de maladie cardio-vasculaire sur 10 ans a été calculé à l'aide de la méthode de notation du risque de Framingham. Le risque de maladie cardio-vasculaire est indiqué en pourcentage du risque et en intervalles de confiance (IC) à 95 %. Les facteurs affectant le risque de maladie cardio-vasculaire ont été évalués au moyen d'une analyse de régression multiple bêta . Résultats : L'âge moyen des participants était de 55,9 ans ; 41 % étaient des hommes. Le risque moyen de développer une maladie cardio-vasculaire sur 10 ans était de 16,4 % (IC à 95 % : 16,0-16,8 %) ; 28,3 % des participants avaient un risque de plus de 20 % (47,8 % des hommes et 14,9 % des femmes). L'âge, le diabète, le tabagisme (uniquement chez les hommes), l'hypertension artérielle, les triglycérides (uniquement chez les femmes), le tour de taille, le cholestérol total et le cholestérol des lipoprotéines de haute densité étaient associés de manière significative au risque de maladie cardio- vasculaire. Chez les hommes, on a constaté une augmentation non significative du risque avec un indice de masse corporelle plus élevé pouvant atteindre 39,9 kg/m2 ; cependant, le risque diminuait de 4,4 % lorsque l'indice de masse corporelle était supérieur ou égal à 40 kg/m2 (p = 0,18). Conclusions : Le risque de maladie cardio-vasculaire était très élevé, surtout chez les hommes. Des interventions efficaces devraient être mises en œuvre pour réduire les facteurs de risque des maladies cardio-vasculaires. Des études longitudinales sont recommandées pour étudier l'effet de l'indice de masse corporelle sur le risque de maladie cardio- vasculaire.

ُّع توقخطر اإلصابة بأمراض القلب واألوعية الدموية ملدة 10 سنوات يف شاهرود بجمهورية إيران اإلسالمية ومتناقضة منسب كتلة اجلسم حممدحسن امامیان، حسن هاشمي، أكرب فتوحي اخلالصة اخللفية: ُيعد تقييم خطر اإلصابة بأمراض القلب واألوعية الدموية ًأمرا ًرضوريا للوقاية من األمراض يف مجيع املناطق. األهداف:هدفت هذه الدراسة إىل ِّتقص خطر اإلصابة بأمراض القلب واألوعية الدموية ملدة 10 سنوات و ُحم ِّدداهتا لدى السكان البالغني يف مدينة شاهرود بجمهورية إيران اإلسالمية. طرق البحث: تم تقييم ما جمموعه 4737 ً شخصاترتاوح أعامرهم بني 45 و69 ًعاما. ُواحت ِ ب سخطر اإلصابة بأمراض القلب واألوعية الدموية ملدة 10 سنوات باستخدام طريقة درجات خماطر فرامنجهام. وتم اإلبالغ بمخاطر اإلصابة بأمراض القلب واألوعية الدموية كنسبة خطر مئوية، وكانت فواصل الثقة بنسبة %95. ُوق ِّيمت العوامل التي ّتؤثر يف خطر اإلصابة بأمراض القلب واألوعية الدموية باستخدام حتليل انحدار بيتا املتعدد. النتائج: بلغ متوسط عمر املشاركني 55.9 ًعاما، وكان %41 منهم من الذكور. وبلغ متوسط خطر اإلصابة بأمراض القلب واألوعية الدموية ملدة 10 سنوات %16.4 )فاصل الثقة %95: 16.0-16.8 ٪(، َّوتعرض ٪28.3 من املشاركني ملخاطر أكثر من ٪20 )٪47.8 من الرجال و 14.9٪ من النساء(. وارتبط العمر ُّوالس َّ ريك والتدخني )لدى الرجال فقط( وارتفاع ضغط الدم وثالثي جليسرييد الدم )لدى النساء فقط( وحميط اخلرص والكوليسرتول ُالك ِّل وكوليسرتول الربوتني الشحمي مرتفع الكثافة بمخاطر اإلصابة بأمراض القلب واألوعية الدموية ٍبصورة كبرية. وحدثت 2 زيادة غري كبرية يف ُّتعرض الرجال للخطر مع ارتفاع منسب كتلة اجلسم إىل 39.9 كجم/م ، ومع ذلك انخفض اخلطر بنسبة %4.4 عند بلوغ منسب كتلة اجلسم ≤ 40 كجم/م2 )القيمة االحتاملية = 0.18(. االستنتاجات:إن خطر اإلصابة بأمراض القلب واألوعية الدموية مرتفع ًجدا، ًخاصة لدى الرجال. وينبغي تنفيذ تدخالت ّفعالة للحد من عوامل خطر اإلصابة بأمراض القلب واألوعية الدموية. َويوص بإجراء دراسات طولية الستقصاء تأثري منسب كتلة اجلسم عىل خطر اإلصابة بأمراض القلب واألوعية الدموية.

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25. Ueda P, Woodward M, Lu Y, Hajifathalian K, Al-Wotayan R, Aguilar-Salinas CA, et al. Laboratory-based and office-based risk scores and charts to predict 10-year risk of cardiovascular disease in 182 countries: a pooled analysis of prospective cohorts and health surveys. Lancet Diabetes Endocrinol. 2017;5(3):196–213. https://doi.org/10.1016/S2213-8587(17)30015-3 26. Gray BJ, Bracken RM, Turner D, Morgan K, Mellalieu SD, Thomas M, et al. Predicted 10-year risk of cardiovascular disease is influenced by the risk equation adopted: A cross-sectional analysis. Br J Gen Pract. 2014;64(627):e634–e40. https://doi.org/10.3399/ bjgp14X681805 27. Yang Q, Zhong Y, Ritchey M, Loustalot F, Hong Y, Merritt R, et al. Predicted 10-year risk of developing cardiovascular disease at the state level in the U.S. Am J Prev Med. 2015;48(1):58–69. https://doi.org/10.1016/j.amepre.2014.09.014 28. Hu FB, Wang B, Chen C, Jin Y, Yang J, Stampfer MJ, et al. Body mass index and cardiovascular risk factors in a rural Chinese population. Am J Epidemiol. 2000;151(1):88–97. https://doi.org/10.1093/oxfordjournals.aje.a010127 29. Khosravi A, Akhavan Tabib A, Golshadi I, Dana Siadat Z, Bahonar A, Zarfeshani S, et al. The relationship between weight and CVD risk factors in a sample population from central Iran (based on IHHP). ARYA Atheroscler. 2012;8(2):82–9. 30. Sepanlou SG, Malekzadeh R, Poustchi H, Sharafkhah M, Ghodsi S, Malekzadeh F, et al. The clinical performance of an of- fice-based risk scoring system for fatal cardiovascular diseases in north-east of Iran. PLoS One. 2015;10(5):e0126779. https://doi. org/10.1371/journal.pone.0126779 31. Hansel B, Roussel R, Elbez Y, Marre M, Krempf M, Ikeda Y, et al. Cardiovascular risk in relation to body mass index and use of evidence-based preventive medications in patients with or at risk of atherothrombosis. Eur Heart J. 2015;36(40):2716–28. https:// doi.org/10.1093/eurheartj/ehv347 32. Appiah D, Schreiner PJ, Durant RW, Kiefe CI, Loria C, Lewis CE, et al. Relation of longitudinal changes in body mass index with atherosclerotic cardiovascular disease risk scores in middle-aged black and white adults: the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Ann Epidemiol. 2016;26(8):521–6. https://doi.org/10.1016/j.annepidem.2016.06.008 33. Romero-Corral A, Montori VM, Somers VK, Korinek J, Thomas RJ, Allison TG, et al. Association of bodyweight with total mortal- ity and with cardiovascular events in coronary artery disease: a systematic review of cohort studies. Lancet. 2006;368(9536):666– 78. https://doi.org/10.1016/S0140-6736(06)69251-9 34. D’Agostino RB Sr, Pencina MJ, Massaro JM, Coady S. Cardiovascular disease risk assessment: insights from Framingham. Glob Heart. 2013;8(1):11–23. https://doi.org/10.1016/j.gheart.2013.01.001 35. Singh SK, Pant B, Davey A, Shukla A, Ahmad S. Dyslipidaemia & Framingham risk score: tools for prediction of cardiovascular diseases as public health problem. Indian J Comm Health. 2016;28(1):45–50. 36. Garg N, Muduli SK, Kapoor A, Tewari S, Kumar S, Khanna R, et al. Comparison of different cardiovascular risk score calcula- tors for cardiovascular risk prediction and guideline recommended statin uses. Indian Heart J. 2017;69(4):458–63. https://doi. org/10.1016/j.ihj.2017.01.015

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Workplace violence among health-care workers in emergency departments of public hospitals in Dammam, Saudi Arabia

Moussa Harthi,1 Mohammed Olayan,1 Hassan Abugad1 and Moataza Abdel Wahab 1

1Department of Family and Community Medicine, Imam Abdulrahman Bin Faisal University, Dammam, Saudi Arabia. (Correspondence to: M.M. Harthi: [email protected]).

Abstract Background: Workplace violence is a serious occupational health problem. Emergency health-care workers have a high risk of exposure to violence with negative personal consequences. Aims: To estimate the prevalence and possible associated factors of workplace violence among health-care workers in emergency departments of public hospitals in Dammam, Saudi Arabia. Methods: A cross-sectional study was conducted during August to October 2018 at 4 emergency departments of public hospitals belonging to the Saudi Ministry of Health. Data were collected using a self-administered questionnaire. Results: Of 380 questionnaires distributed, 324 were returned (85% response rate). Almost two thirds of the participants were women (66.4%) and more than half (54%) were nurses. A total of 155 health-care workers (47.8%) had experienced at least 1 type of violent incident in the preceding 12 months. Of the total violence incidents, 52% were verbal abuse, 19% were physical violence, and sexual harassment (3%) was the least common. Lack of encouragement to report incidents and Sau- di nationality were the only significant variables associated with workplace violence. Conclusions: Workplace violence was prevalent, and verbal abuse was the commonest type among health-care workers in emergency departments of Saudi hospitals. Encouragement to report violent incidents and raising awareness among health-care workers about violence reporting systems are important strategies to improve workplace safety. Keywords: emergency departments, healthcare workers, Saudi Arabia, reporting, workplace violence Citation: Harthi M; Olayan M; Abugad H; Abdel Wahab M. Workplace violence among health-care workers in emergency departments of public hospi- tals in Dammam, Saudi Arabia. East Mediterr Health J. 2020;26(12):1473–1481. https://doi.org/10.26719/emhj.20.069 Received: 30/05/19; accepted: 19/11/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction force, against another person or group that can result in harm to physical, mental, spiritual, moral or social devel- Health care workers (HCWs) are among the groups most opment. Psychological violence includes verbal abuse, experiencing violence and aggressive behaviour at work, bullying/mobbing, harassment (including sexual and ra- especially those who work in emergency departments cial) and threats. (EDs) in public hospitals (1). Workplace violence has neg- ative consequences on safety and workplace activities of Many studies worldwide have examined the HCWs (2). However, the estimated prevalence of violence prevalence of workplace violence among HCWs (2). A against HCWs is still unknown because there is no clear survey of workplace violence across 65 American EDs definition of a violent incident (1,2). The World Health conducted in 2008 showed that the violence and weapons Organization (WHO) defined violence as “The intention- in the EDs were common, and nurses were less likely al use of physical force or power, threatened or actual, to feel safe than other staff were (6). A cross-sectional against another person or against oneself or a group of study in 2009 in Tokyo, Japan revealed that 36.4% of people that results in or has a high likelihood of resulting 11 095 HCWs in 19 hospitals experienced workplace in injury, death, psychological harm, maldevelopment or violence by patients or their relatives; 15.9% experienced deprivation” (3). The National Institute for Occupational physical aggression, 29.8% experienced verbal abuse Safety and Health defines workplace violence as “violent and 9.9% experienced sexual harassment (7). In another acts (including physical assault and threats of assault) di- large study conducted between October 2012 and July rected towards persons at work or on duty” (4). According 2013 at primary healthcare centres in Belgrade, Serbia, to WHO, physical or psychological violence can appear in the prevalence of workplace violence was 52.6% among different forms, which may often overlap (4,5). Physical 1757 HCWs (8). In the Middle East, workplace violence violence is defined as the use of physical force against has been investigated in several studies. An Iranian another person or group that results in physical, sexual cross-sectional survey in 2011 among 196 nurses in 11 or psychological harm, and such violence includes beat- EDs in teaching hospitals in Tehran, showed that 19.7% ing, kicking, slapping, stabbing, shooting, pushing, bit- of nurses faced physical violence and 91.6% experienced ing and pinching (3,5). Psychological violence is defined verbal abuse (9). Another cross-sectional study in Jordan as intentional use of power, including threat of physical in 2011 among 227 nurses in 12 provinces revealed that

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75.8% were exposed to at least 1 type of violence (10). A a self-administered questionnaire that was based on comprehensive survey of workplace violence among questionnaires developed by WHO (5) and was modified 713 physicians in EDs in Turkey found that 78.1% had by the researchers. The English language questionnaire experienced violence (11). Factors related to the increased was translated into Arabic by the authors and validated the risk of workplace violence are related to the offenders, by 3 experts in the Department of Family and Community HCWs or the workplace environment (2). Personality and Medicine, Imam Abdulrahman Bin Faisal University. mental health disorders (such as schizophrenia, paranoia, The questionnaire consisted of 8 sections. The first part anxiety, antisocial attitude, dementia and alcohol abuse) included demographic information such as age, sex, are the most significant factors related to the offenders marital status, occupational title, nationality, educational (7). HCW-related factors include understaffed working level, and years of work experience. The second conditions, working alone and long working hours (7, part consisted of items that addressed occupational 12). Factors related to the workplace include long waiting characteristics (working multiple shifts, shift time times, overcrowding, inadequate security, and lack of worked, number of coworkers in the same work area, policies for preventing violence (12). In a few studies encouragement to report violent events, and availability in Saudi Arabia, there was difficultly in estimating the of a violence reporting system). The other sections magnitude of the problem due to lack of reporting and consisted of items that addressed the characteristics of other factors (2,13). In 2009, a self-reporting questionnaire the violent acts experienced (time, place and frequency study in Al-Hassa of 1091 primary health care professionals of violence) and the identity, age and sex of the offender. revealed that 28% suffered from workplace violence (12). A There were also questions about reasons for violence cross-sectional study in Riyadh in 2011 of 600 physicians (e.g., lack of security and absence of punishment) and the and nurses found that 67.4% were exposed to workplace consequences for the HCWs and the offenders. Finally, violence, and that nurses were more susceptible than there was a question about reasons for not reporting physicians (14). In another cross-sectional study in 2014 in acts of violence. Types of violence were classified 12 family medical centres in Riyadh, 45.6% of 270 HCWs into physical, verbal, bullying, and sexual and racial experienced some sort of violence during the 12 months harassment (5). A pilot study was carried out on 10 HCWs prior to the study (2). Three studies were conducted in in 1 public hospital on 1 day, to check the clarity of the Saudi Arabia in 2015. A cross-sectional study at King Fahd language used and estimate the average time to answer Hospital showed that 30.7% of 391 nurses were exposed to the questionnaire. The participants in the pilot study verbal abuse (13). In EDs of 3 hospitals in Riyadh, 89.3% of were not included in the present study. 121 nurses experienced a violent incident in the 12 months All statistical analyses were conducted using SPSS prior to the study (15). In EDs in Tabuk, 90.7% of 129 had version 25, setting our level of confidence at 95%. history of workplace violence (1). EDs are in operation 24 Descriptive statistics by frequency and percentage hours a day, 7 days a week (16). Patients usually come to were used for categorical variables, while continuous EDs with relatives or friends with expectations of a rapid variables were assessed for normality. The frequency response and good service from HCWs regardless of the of workplace violence was calculated by dividing the severity of the case (12). EDs receive a huge number of number of those who had experienced violence during patients, therefore, the chance of HCWs being exposed to the preceding 12 months by the total number of HCWs violence is high (1,12). in the study. The c2 and independent samples t test This study was conducted to estimate the prevalence were used to assess the relation between demographic of workplace violence among HCWs in EDs in public and occupational characteristics and workplace hospitals in Dammam, Saudi Arabia and to determine violence. Logistic regression analysis was used to assess possible associated factors. factors independently associated with the occurrence of workplace violence. Adjusted odds ratios with Methods corresponding 95% confidence intervals were presented. This was a cross-sectional survey conducted during Au- Results gust to October 2018 at 4 public hospitals belonging to the Ministry of Health in Dammam, Saudi Arabia: Dam- Demographic and occupational characteristics mam General Medical Complex, Dhahran Eye Specialist Of 380 questionnaires distributed, 324 were returned (85% Hospital, Maternal and Children’s Hospital and Al-Amal response rate). The age of participants ranged between 22 Complex for Mental Health). All HCWs in all duty shifts and 55 years, with a mean of 32.7 (standard deviation, 6.2) (morning, evening and night) in EDs were invited to par- years, and 215 were women (66.4%) (Table 1). The majority ticipate, with exclusion of those with work experience < (78.1%) of HCWs were Saudis and almost two thirds were 1 year. The sample size was calculated using epi info, as- married. The largest proportion had a diploma (50.3%) fol- suming the level of violence among HCWs was 89% from lowed by a bachelor’s degree (43.5%). More than half the previous data (15), with an accepted margin of error 4%. HCWs (54%) were nurses and 40.1% had work experience The sample by population survey was 235 HCWs at 95% of 6–9 years. confidence level and was increased to 294 HCWs, expect- ing 80% response. Report encouragement and system availability Data were collected from 324 participants, using One hundred and ninety-three (59.6%) of 324 respondents

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Table 1 Demographic and occupational characteristics of and 73 (30.3%) more than once a month. Most (n = 102, health-care workers in emergency departments 42%) of the offenders were patients, followed by relatives Health-care worker characteristics No. % of patients (n = 75, 31%). The majority (n = 197, 82%) of the Occupation offenders were aged 21–45 years and 41 (17%) were ≥ 46 Physician 63 19 years. Both men and women committed the violent act Nurse 175 54 in 97 (40.25%) cases, men only in 95 (39.42%) and wom- Othersa 86 27 en only in 49 (20.33%). Most (n = 180, 74.7%) of the par- Sex ticipants exposed to violence believed that the incident Male 109 33.6 could have been prevented. The violence incident ended Female 215 66.4 with the following consequences for the offenders: none b Age (yr) (n = 154, 63.9%), verbal warning (n = 51, 21.2%) and reported ≤ 30 153 47.2 31–40 136 42 to the police (n = 16, 6.6%). The consequences for HCWs > 40 35 10.8 were: none (n = 112, 46.5%), reduced work performance (n Marital status = 107, 44.4%), documented complaint against HCWs (n = Married 226 69.8 20, 8.3%) and injuries (n =2, 0.8%). Almost all (n = 41, 91.1%) Unmarried 98 30.2 incidents of physical violence happened without a weap- Nationality on and 23 (51.1%) were committed by men. Most physical Saudi 253 78.1 (n =22, 48.9%) and verbal abuse (n = 55, 43.7%) occurred Non-Saudi 71 21.9 in the evening. The majority (n = 29, 74.4%) of bullying Education incidents occurred in the morning and managers were a Diploma 163 50.3 major source (n = 22, 56.4%) of violent incidents, followed Bachelor’s 141 43.5 by staff members (n = 14 ,35.9%). In 34 (87.2%) of those in- Master’s 12 3.7 Boardc 8 2.5 cidents, no action was taken. Sexual harassment among staff members was the highest (n = 3, 42.9%). Decline in Work experience (yr) 1–5 126 38.9 work performance was reported in 20 (44.4%) HCWs who 6–9 130 40.1 experienced physical violence and in 13 (54.2%) who were > 10 68 21 subjected to racial harassment. Multiple shifts Yes 292 90.1 Factors associated with workplace violence No 32 9.9 HCWs who experienced violence reported that it was Shift time caused by absence of punishment (67%), lack of security Morning 42 13 (51%), staff shortage (34%), long waiting time for patients Alternate 282 87 (33%), overcrowding (29%), personality type (17%), cultural No. of coworkers beliefs (9%), lack of patient privacy (3%) and language bar- Mean (standard deviation) 9 (5) ≤ 10 232 71.6 rier (2%). Absence of punishment was the most common > 10 92 28.4 cause of verbal abuse (61%), bullying (95%), sexual (71%) aPharmacists, technicians and clerical workers. and racial (58%) harassment, whereas, lack of security bMean age 32.7 (6.2) years. was the most common cause of physical violence (64%). cMedical degree for physicians to receive privileges and to practice medicine in a particular field. History of workplace violence related to characteristics of health-care workers Demographic and occupational features of HCWs who stated that they were encouraged to report workplace did and did not experience violence are shown in Table violence and 131 (40.4%) that they were not encouraged. 3. Sex was significantly associated with violence, with vi- Two hundred and twenty-five (69.4%) HCWs reported olence being more frequent for men (n = 63, 57.8%) than that a system was available for reporting violence and 99 women (n = 92, 42.8%). Nationality was significantly as- (30.6%) reported no such system. sociated with violence and was more frequent for Saudis Frequency and type of violent incident (n = 131, 51.8%) than non-Saudis (n = 24, 33.8%). Those who worked with ≤ 10 coworkers (n = 124, 53.4%) reported sig- Out of 324 HCWs, 155 (47.8 %) had experienced at least 1 nificantly more frequent violence than those who worked type of violent incident during the preceding 12 months. with > 10 coworkers (n = 31, 33.7%). Those who lacked en- Among 241 incidents, 126 (52%) were verbal abuse, 45 couragement to report violent acts (n = 79, 60.3%) report- (19%) physical violence, 39 (16%) bullying, 24 (10%) racial ed significantly more frequent violence than those who harassment and 7 (3%) sexual harassment (Table 2). Nine- had such encouragement (n = 76, 39.4%). Those who con- ty-five (39.4%) violent incidents happened in the morning firmed lack of availability of a system for reporting vio- and the same number in the evening. Almost all (n = 232, lence (n = 57, 57.6%) reported significantly more frequent 96.3%) of the violent incidents occurred in the workplace. violence than those who confirmed system availability Ninety-nine (41.1%) violent incidents occurred once a year (n= 98, 43.6%).

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Table 2 Characteristics and types of workplace violence among health-care workers in emergency departments Characteristics and types of violence Physical Verbal Bullying Sexual Racial Total n % n % n % n % n % n % 45 19 126 52 39 16 7 3 24 10 241 100 Shift time Morning 10 22.2 42 33.3 29 74.4 3 42.9 11 45.8 95 39.4 Evening 22 48.9 55 43.7 6 15.4 3 42.9 9 37.5 95 39.4 Night 13 28.9 29 23 4 10.3 1 14.3 4 16.7 51 21.2 Location Inside 40 88.9 123 97.6 38 97.4 7 100 24 100 232 96.3 Outside 0 0 1 0.8 1 2.6 0 0 0 0 2 0.8 Both 5 11.1 2 1.6 0 0 0 0 0 0 7 2.9 Frequency a Once a year 24 53.3 39 31 21 53.8 5 71.4 10 41.7 99 41.1 Once a month 14 31.1 39 31 9 23.1 0 0 7 29.2 69 28.6 More than once per month 7 15.6 48 38 9 23.1 2 28.6 7 29.2 73 30.3 Offender identity Patient / client 24 53.3 65 51.6 0 0 2 28.6 11 45.8 102 42 Relatives 16 35.6 48 38.1 0 0 1 14.3 10 41.7 75 31.1 Staff memberb 1 2.2 5 4 14 35.9 3 42.9 0 0 23 10 Management 0 0 1 0.8 22 56.4 0 0 3 12.5 26 10.8 External colleague 1 2.2 1 0.8 3 7.7 0 0 0 0 5 2 General public 3 6.7 6 4.8 0 0 1 14.3 0 0 10 4.1 Offender age < 20 years 0 0 3 2.4 0 0 0 0 0 0 3 1 21–45 years 42 93.3 100 79.4 30 76.9 7 100 18 75 197 82 ≥ 46 years 3 6.7 23 18.3 9 23.1 0 0 6 25 41 17 Offender sex a Male 23 51.1 40 32 18 46.2 5 71.4 9 37.5 95 39.42 Female 7 15.6 24 19 11 28.2 2 28.6 5 20.5 49 20.33 Both 15 33.3 62 49 10 25.6 0 0 10 41.7 97 40.25

Could have been prevented Yes 41 91.1 91 72.2 28 71.8 4 57.1 16 66.7 180 74.7 No 4 8.9 35 27.8 11 28.2 3 42.9 8 33.3 61 25.3 Consequences on attacker None 19 42.2 80 63.5 34 87.2 4 57.1 17 70.8 154 63.9 Verbal warning 13 28.9 29 23 2 5.1 3 42.9 4 16.7 51 21.2 Reported to police 9 20 7 5.6 0 0 0 0 0 0 16 6.6 Do not know 4 8.9 10 7.9 3 7.7 0 0 3 12.5 20 8.3 Consequences on HCW None 16 35.6 61 48.4 20 51.3 5 71.4 10 41.7 112 46.5 Reduce work performance 20 44.4 54 42.9 18 46.2 2 28.6 13 54.2 107 44.4 Incident form against HCWs 7 15.6 11 8.7 1 2.6 0 0 1 4.2 20 8.3 Injured 2 4.4 0 0 0 0 0 0 0 0 2 0.8 aPercentage calculated from HCWs that could have been subjected to > 1 incidence of violence. bPhysicians, nurses, pharmacists, technicians and clerical workers. HCW = healthcare worker.

Type of workplace violence related to 7.6%). Verbal abuse was also significantly more frequent characteristics of health-care workers in HCWs with < 10 coworkers (n = 101, 43.5%) than in those with > 10 coworkers (n = 25, 27.2%). HCWs who lacked en- Men (n = 22, 20.2%) experienced significantly more couragement to report violent incidents reported signifi- physical violence than women did (n = 23, 10.7%) (Table cantly more verbal abuse (n = 65, 49.6%) than those who 4). Men (n = 51, 46.8%) also had significantly more verbal had encouragement (n = 61, 31.6%). Similarly, HCWs who abuse than women had (n =75, 34.9%). Violence was sig- lacked encouragement to report violence reported signif- nificantly more frequent for unmarried n( = 5, 5.1%) than icantly more bullying (n = 23, 17.6%) than those who had married (n =2,0.9%) HCWs. Saudi HCWs (n = 106, 41.9%) encouragement (n = 16, 8.3%). In contrast, demographic experienced verbal abuse significantly more often than and occupational characteristics, such as age, occupation, non-Saudis did (n = 20, 28.2%). Physical violence was sig- shift time, direct contact with patient, and patient types, nificantly more frequent in HCWs with < 10 coworkers were not significantly associated with general or specific (n = 38,16.4%) than in those with > 10 coworkers (n = 7, types of violence.

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Table 3 History of workplace violence related to characteristics of health-care workers in emergency departments Health-care worker characteristics History of exposure to violence Total c2 P 324 Yes No n % n % n % Sex Male 63 57.8 46 42.2 109 33.6 6.528 0.01 Female 92 42.8 123 57.2 215 66.4 Age 155 169 324 0.622 Mean (SD) 32.5 (5.7) 32.9 (6.6) Age group, yr ≤ 30 70 45.8 83 54.2 153 47.2 31–40 71 52.2 65 47.8 136 42 2.168 0.338 > 40 14 40 21 60 35 10.8 Marital status Married 109 48.2 117 51.8 226 69.8 0.046 0.831 Unmarried 46 46.9 52 53.1 98 30.2 Nationality Saudi 131 51.8 122 48.2 253 78.1 7.179 0.007 Non-Saudi 24 33.8 47 66.2 71 21.9 Occupation Physician 34 54 29 46 63 19 Nurse 84 48 91 52 175 54 1.75 0.417 Others 37 43 49 57 86 27 Shift time Morning 17 40.5 25 59.5 42 13 1.048 0.306 Alternate 138 48.9 144 51.1 282 87 No. of coworkers ≤ 10 124 53.4 108 46.6 232 71.6 10.3 0.001 > 10 31 33.7 61 66.3 92 28.4 Report encouragement Yes 76 39.4 117 60.6 193 59.6 13.69 <0.001 No 79 60.3 52 39.7 131 40.4 System availability Yes 98 43.6 127 56.4 225 69.4 5.41 0.02 No 57 57.6 42 42.4 99 30.6

SD = standard deviation.

Logistic regression analysis of workplace and 10 primary healthcare centres in Saudi Arabia who violence experienced at least 1 violence incident (22), and similar to the prevalence of 45.6% among HCWs in 12 family medi- After entering sex, nationality, number of coworkers, lack cal centres in Riyadh (2). of report encouragement and system availability into the regression model, the only independent variables signif- Most studies have shown that psychological violence icantly associated with general violence were lack of re- (especially verbal abuse) was higher than physical violence port encouragement and Saudi nationality (Table 5). For (15,21,26). The number of incidents of verbal abuse was physical violence, the only significant independent factor approximately 5-fold that of the number of incidents of was male sex. Lack of report encouragement was the only physical violence among nurses in several EDs in Jordan variable that remained significantly associated with ver- (10), which can be explained by the stress of acute illness bal abuse and bullying. experienced by patients and/or families at the time of the violent act. In the current study, verbal abuse formed 52% Discussion of the violent incidents, physical violence 19%, bullying The main aim of this study was to estimate the prevalence 16%, racial harassment 10% and sexual harassment was of workplace violence in a sample of 324 participants the least common (3%). Similarly, a study in Macau working in EDs in 4 public hospitals in Dammam, Saudi revealed incidents of verbal abuse (53.4%), physical Arabia. The study showed that the prevalence of violence assault (16.1%), bullying (14.2%), sexual harassment (4.6%) among HCWs was 47.8%, which was considerably lower and racial harassment (2.6%) among physicians and than 89.3% in nurses in the EDs in 3 public hospitals in nurses (24). Verbal abuse was the most common form Saudi Arabia (15). However, our result was closer to the of violence because it was easy to perpetuate and could prevalence of 57.5% in HCWs in 2 government hospitals not be controlled by any sort of security measures. The

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Table 4 Type of workplace violence related to characteristics of health-care workers in emergency departments Health-care worker characteristics Physical Yes % No % Total c2 P 324 Sex Male 22 20.2 87 79.8 109 5.442 0.02 Female 23 10.7 192 89.3 215 No. of coworkers ≤ 10 38 16.4 194 83.6 232 4.237 0.04 > 10 7 7.6 85 92.4 92 Verbal Sex Male 51 46.8 58 53.2 109 4.314 0.038 Female 75 34.9 140 65.1 215 Nationality Saudi 106 41.9 147 58.1 253 4.397 0.036 Non-Saudi 20 28.2 51 71.8 71 No. of coworkers ≤ 10 101 43.5 131 56.5 232 7.420 0.006 > 10 25 27.2 67 72.8 92 Report encouragement Yes 61 31.6 132 68.4 193 10.653 0.001 No 65 49.6 66 50.4 131 Bullying Report encouragement Yes 16 8.3 177 91.7 193 6.329 0.012 No 23 17.6 108 82.4 131 Sexual Marital status Married 2 0.9 224 99.1 226 0.028 Unmarried 5 5.1 93 94.9 98

SD = standard deviation. majority (74.4%) of bullying incidents occurred in the absence of punishment, lack of security, and long waiting morning and managers were a major source (56.7%) of times for patients. Certain characteristics of HCWs, incidents followed by staff members (35.9%), which is including age, sex, years of experience and marital status, often explained by the presence of most managerial staff have been associated with increased workplace violence in the morning. Moreover, interprofessional violence (27,28). In the current study, the frequency of physical may have played a role in these incidents. violence was high among men (20.2%) and sexual Most of the workplace violence was experienced by harassment was high among unmarried HCWs (5.1%). Saudi nationals, which is explained mainly by the high More than half of violent incidents (66.7 %) were number of Saudi participants in the study. The majority of not reported and the main reason was the feeling that offenders were patients (42%) followed by their relatives reporting was useless. This could be related to the (31%), which was similar to some previous studies existing system that includes reporting the incident to a (2,15,20,25,26) but contrary to others (1,14,23), in which the supervisor, duty director, or the police. Most HCWs (n = companions of the patients were the main offenders. The 57, 57.6%) exposed to workplace violence questioned the fact that patients were the major aggressors in the current availability of a violence reporting system. Moreover, study could be explained by the absence of deterrent the majority (75.9%) raised queries about the efficiency action (63.9%) towards violent incidents as supported by of the security measures applied in EDs of the studied management in the workplaces, following the rule “the hospitals. Our results could be explained by lack of patient is always right”. awareness of the reporting systems and inefficient Workplace violence had negative consequences security measures. Hogarth et al. (29) noted that the on HCWs, such as reduced work performance (44.4%), solution agreed upon by HCWs to decrease workplace complaints against HCWs (8.3%) and injuries (0.8%), violence was encouragement by management to report which is supported by previous studies (1,2,18,19). Reduced violent incidents and to develop preventative measures. work performance could be explained by feeling unsafe, The current study is one of few to cover all types of anger, anxiety or distress or performing duties in an violence (physical and psychological, including verbal unprofessional way. Some previous studies suggested threats, bullying, and sexual and racial harassment) that the reasons for violence in EDs were staff shortage, and used the standard WHO definition of violence.

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Table 5 Logistic regression analysis of workplace violence using significantly associated characteristics of health-care workers in emergency departments Variables B SE Wald df Sig Exp(B) 95% CI test for Exp(B) Lower Upper General Saudi nationality 1.015 0.438 5.375 1 0.020 2.759 1.170 6.507 Lack of report encouragement -0.915 0.375 5.945 1 0.015 2.497 1.197 5.209 Constant -0.351 0.723 0.236 1 0.627 0.704 Physical Male sex 1.045 0.485 4.632 1 0.031 2.842 1.098 7.358 Constant -2.380 0.331 51.824 1 < 0.001 0.093 Verbal Lack of report encouragement 0.887 0.425 4.350 1 0.037 2.428 1.055 5.589 Constant -2.260 0.595 14.448 1 <0.001 0.104 Bullying Lack of report encouragement 0.857 0.348 6.074 1 0.014 2.356 1.192 4.657 Constant -3.260 0.570 32.676 1 < 0.001 0.038 df = degrees of freedom; SE = standard error; Sig = significance.

Additionally, all HCWs in EDs of public hospitals were ment, which was agreed upon by the majority of HCWs. targeted. However, limitations cannot be excluded. The Creation of an environment that encourages HCWs to size of the sample may limit generalization of the results. report violent incidents and raising awareness of HCWs The questionnaire was self-administered and recall bias about violence reporting systems in EDs are recommend- could not be excluded, as in most similar surveys. ed. Ensuring the reporting of all violent incidents and follow-up of the appropriate actions are essential. Sup- Conclusions and recommendations porting programmes to help and provide HCWs with the knowledge to manage and control incidents are needed. In this study, workplace violence was prevalent among HCWs, and verbal abuse was the commonest type. The Funding: None. most important associated factor was absence of punish- Competing interests: None declared.

Violence au travail chez les agents de santé œuvrant dans les services d’urgence des hôpitaux publics de Dammam, en Arabie saoudite Résumé Contexte : La violence est un grave problème de santé au travail. Les agents de santé des services d’urgence sont particulièrement susceptibles d’être exposés à la violence et d’en subir les conséquences négatives sur le plan personnel. Objectifs : La présente étude visait à estimer la prévalence de la violence au travail et des facteurs qui y sont potentiellement associés chez les agents de santé œuvrant dans les services d’urgence des hôpitaux publics de Dammam, en Arabie saoudite. Méthodes : Une étude transversale a été menée d’août à octobre 2018 dans quatre services d’urgence d’hôpitaux publics relevant du ministère saoudien de la Santé. Les données ont été recueillies au moyen de questionnaires auto-administrés. Résultats : Sur les 380 questionnaires distribués, 324 ont été renvoyés (taux de réponse de 85 %). Près des deux tiers des participants étaient des femmes (66,4 %) et plus de la moitié (54 %) étaient des infirmières. Au total, 155 agents de santé (47,8 %) ont subi au moins un type de violence au cours des 12 mois précédents. Sur l’ensemble des faits de violence signalés, 52 % étaient des violences verbales et 19 % des violences physiques. Le harcèlement sexuel (3 %) était le type de violence le moins fréquent. Le manque d’encouragement à signaler les actes de violence et la nationalité saoudienne étaient les seules variables significatives associées à la violence sur le lieu de travail. Conclusions : La violence sur le lieu de travail est répandue. Les violences verbales sont les faits les plus fréquemment rapportés par les agents de santé œuvrant dans les services d’urgence des hôpitaux saoudiens. Pour améliorer la sécurité sur le lieu de travail, il est important d’encourager les agents de santé à signaler les faits de violence et de leur faire connaître les mécanismes qui leur permettent de le faire.

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العنفيف أماكن العمل بني العاملني يف جمال الرعاية الصحية يف أقسام الطوارئ باملستشفيات العامة يف الدمام باململكة العربية السعودية موسى احلارثي، حممد عليان، حسن أبوجد، معتزة عبد الوهاب اخلالصة اخللفية: ُعد يالعنف يف مكان العمل أحد مشاكل الصحة املهنية اخلطرية. ويواجه العاملون يف جمال الرعاية الصحية الطارئة ًخطرا ًكبريا ُّللتعرض للعنف مع عواقب شخصية سلبية. األهداف:هدفت هذه الدراسة إىل تقدير معدل انتشار العنف يف مكان العمل بني العاملني يف جمال الرعاية الصحية يف أقسام الطوارئ يف املستشفيات العامة يف الدمام باململكة العربية السعودية، والعوامل املحتملة املرتبطة به. طرق البحث: ُجريت أدراسة مقطعية خالل الفرتة من أغسطس/آب إىل أكتوبر/ترشين األول 2018 يف 4 أقسام طوارئ يف املستشفيات العامة التابعة لوزارة الصحة السعودية. ُوجعت البيانات من خالل استبيان يملؤه املستجيبون بأنفسهم. النتائج:من االستبيانات َّاملوزعة البالغ عددها 380 ً،استبيانا تم الرد عىل 324 منهم )بمعدل استجابة (.%85 وكان ثلثا املشاركني ًتقريبا من النساء )%66.4(، وكان أكثر من نصفهم )%54( من طواقم التمريض. وقد َّتعرض ما جمموعه من155 العاملني يف جمال الرعاية الصحية )%47.8( لنوع واحد عىل األقل من حوادث العنف خالل اإلثنى عرش ًشهرا السابقة. ومن جمموع حوادث العنف، كان ٪52 منها حوادث إساءة لفظية، و19٪ حوادث عنف بدين، وكان التحرش اجلنيس )٪ (3 األقل ً.وكان شيوعاعدم التشجيع عىل اإلبالغ عن احلوادث واجلنسية السعودية املتغريات املهمة الوحيدة املرتبطة بالعنف يف مكان العمل. االستنتاجات:إن العنف يف مكان العمل منترش، وكانت اإلساءة اللفظية النوع األكثر ًبني شيوعاالعاملني يف جمال الرعاية الصحية يف أقسام الطوارئ يف املستشفيات السعودية. ُعد ويالتشجيع عىل اإلبالغ عن حوادث العنف وإذكاء الوعي بني العاملني يف جمال الرعاية الصحية بشأن ُظمن اإلبالغ عن العنف من االسرتاتيجيات املهمة لتعزيز السالمة يف مكان العمل.

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Access to health care for patients with thalassaemia in Greece: a cross-sectional study

Kyriakos Souliotis,1,2 Christina Golna,3 Sofia Nikolaidi,2 Georgia Vatheia 2 and Stanimir Hasurdjiev 4

1Department of Social and Education Policy, University of Peloponnese, Corinth, Greece. 2Health Policy Institute, Athens, Greece. 3Innowth Limited, Larnaca, Cyprus. 4Patient Access Partnership, Brussels, Belgium. (Correspondence to: Kyriakos Souliotis: [email protected]; [email protected]).

Abstract Background: The prevalence and clinical burden of beta-thalassaemia in Greece is high. Little information is available on the unmet needs of patients with beta-thalassaemia and barriers to access to care. Aims: This study investigated barriers that patients with transfusion-dependent beta-thalassaemia in Greece face when accessing care and the associations between socioeconomic factors and access to care. Methods: A cross-sectional study was conducted between November 2018 and January 2019. The sample consisted of 116 beta-thalassaemia patient-members of two Panhellenic patient associations for people with thalassaemia. All respond- ents were transfusion-dependent. The survey customized and used the Patient Access Partnership 5As of access tool to measure participants’ access to health care services (subscales: accessibility, adequacy, affordability, appropriateness and availability). Data on their socioeconomic characteristics were also recorded. The association between the total score of each subscale and patient characteristics was examined using the Mann–Whitney or Kruskal–Wallis tests. Results: Respondents considered inpatient services less adequate and appropriate, and outpatient services and labora- tory tests less affordable. Outpatient services were also perceived as less available. Participants’ income was statistically significantly associated with all the subscales except accessibility, and rural residence was significantly associated with all five subscales. Conclusion: Barriers in access to health care among beta-thalassaemia patients receiving transfusions still persist, espe- cially for those who live far from transfusion centres and have lower incomes. It is important to understand and map cur- rent unmet medical and social needs of beta-thalassaemia patients in Greece, in order to design and implement a targeted health policy that can measurably improve patients’ lives. Keywords: beta-thalassaemia, transfusion, health services accessibility, socioeconomic factors, Greece Citation: Souliotis K; Golna C; Nikolaidi S; Vatheia G; Hasurdjiev S. Access to health care for patients with thalassaemia in Greece: a cross-sectional study. East Mediterr Health J. 2020;26(12):1482–1492. https://doi.org/10.26719/emhj.20.118 Received: 01/11/19; accepted 19/03/20 Copyright © World Health Organization (WHO) 2020. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https:// creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction According to the National Registry for Haemoglobin- opathies in Greece, among 4032 patients registered, the Management of beta-thalassaemia major includes regu- peak distribution among thalassaemia major patients is lar blood transfusions and iron chelation therapy to man- the 36–45-year-old age group (8). The prognosis for trans- age iron overload in the body (1,2). Allogeneic haemato- fusion-dependent beta-thalassaemia patients in Greece poietic stem cell transplantation is the only definitive has changed with transfusions and chelation therapy, cure for transfusion-dependent young patients before from being fatal in early childhood to becoming a chronic the development of iron-related tissue damage (3). New disorder with prolonged survival (9). therapies are currently in development for the treatment Despite regular transfusion and chelation therapy, of anaemia and iron overload based on the correction of patients with thalassaemia have an increased mortality the pathophysiological mechanisms of the disease (4). rate compared with the general population (10). Heart In Greece, the mean prevalence of beta-thalassaemia disease is the most common cause of death, accounting is estimated at 7.4%. Its distribution is very uneven and for 51.0% of total deaths in patients with thalassaemia frequencies as high as 15% have been reported in certain between 2000 and 2010 and 28.1% between 2010 and 2015 geographic areas (5). For example, in Halkidiki, of 3931 (8,11). The age of death from heart disease was higher after hospitalized patients screened for haemoglobinopathies, 2005 than before 2005 (8). 10.8% were identified as heterozygotes for beta- Amid the economic crisis in Greece, reduced thalassaemia (6). Equally, molecular analysis of 199 resources have had a negative impact on access to health unrelated patients in south-western Greece confirmed care services mostly due to increases in demand, waiting distinct distribution patterns of specific mutations of the times and co-payments and the decreased ability to pay HBB gene in the Achaia and Ilia prefectures (7). for informal payments (12). As ability to pay declines,

1482 Research article EMHJ – Vol. 26 No. 12 – 2020 access to care becomes a critical issue, particularly for low- Data collection tool income and vulnerable groups (13). A series of previous A questionnaire with the following subsections was de- studies investigated the impact of decreased ability to veloped. pay, due to the economic crisis, in several patient groups, such as patients with rheumatoid arthritis (14), multiple • Participant characteristics: This section recorded sclerosis (15) and cancer (16). These studies confirmed that anonymized data on the sociodemographic (sex, age, most patients had considerable difficulty in accessing education and marital status) and socioeconomic characteristics (source of income, self-evaluation of medication, with the most common barriers to treatment financial status and profession) of the participants being low income, geographical distance from a physician, and their health insurance. long waiting lists and a complicated prescription process, in combination with the low availability of medicines • 5As questionnaire to assess access: We customized in the national health service hospitals. Inequalities and used the Patient Access Partnership 5As in access were also evident in intravenous drug users, framework for measuring access to health care diagnosed with hepatitis C virus (17). services (24) as a composite tool to measure all elements of access to services related to transfusion Given these findings, and considering the high (accessibility, adequacy, affordability, appropriateness prevalence and clinical burden of beta-thalassaemia and availability) among our transfusion-dependent in Greece, the high cost of blood in the country (18,19) beta-thalassaemia participants. and current blood shortages (20,21), we aimed to assess barriers in access to health care services among patients We defined the transfusion burden as the sum of with transfusion-dependent thalassaemia in Greece. the burden on the patient and his/her family of each of the following six types of health care services related to Methods having transfusions: (i) transfusion (the actual process), (ii) general health services (outpatient), (iii) general health Study design services (inpatient), (iv) medications (prescription), We conducted a descriptive, observational cross-section- (v) medications (dispensing) and (vi) laboratory tests. al study. Data were collected during a 3-month period, be- We evaluated each of these elements against the 5As. All tween November 2018 and January 2019. items are rated on 5-point Likert scale ranging from 0 (not at all) to 4 (very). Study population and procedures Two bilingual translators translated the scale from Our study sample consisted of beta-thalassaemia pa- English to Greek and back-translated to ensure that the tients, who were members of two thalassaemia patient Greek version was equivalent to the original English associations, the Greek Thalassaemia Federation, which questionnaire. The questionnaire was then piloted is an umbrella organisation for all thalassaemia patient in 30 patients for content and linguistic clarity. The associations, and the Panhellenic Association for Patients results of the pilot study and the content validity of the with Thalassaemia which is the largest thalassaemia pa- questionnaire were evaluated by a group of experts. tient association in the country. The health care system in Patients who participated in the pilot phase were Greece is centralized and patient associations are most- excluded from the final analysis. ly located in Athens, but their members live all over the Statistical analysis country (22); therefore, our sample can be considered a national sample. We calculated the Cronbach alpha for each of the five subscales (accessibility, adequacy, affordability, appropri- We used purposive sampling (23) to select study ateness and availability) to assess internal consistency. As participants, as people with beta-thalassaemia are all continuous variables were not normally distributed, a special treatment group. We sent an email to the we calculated the medians and interquartile range (IQR). president of the board of directors of each association We used the Kolmogorov–Smirnov criterion to check for along with the study’s protocol and instrument for normality as well as graphical representation. For cate- approval. Both patient associations agreed to participate gorical variables (sex, residence, educational level, age, in the study. Each patient association sent a participation marital status, income, profession, source of income, invitation, an informed consent form, information on health insurance status and self-evaluation of financial the study and a link to the questionnaire to its members. status), we calculated absolute and relative frequencies. The email clearly stated that patients not currently We examined the association between the total score of undergoing transfusion were not eligible to participate. each subscale and patient characteristics in a univariate All members aged 18 and over, who were diagnosed with analysis using the Mann–Whitney U test or Kruskal– beta-thalassaemia and were transfusion-dependent at Wallis test with Dunn pairwise tests adjusted using Bon- the time of the study were eligible to participate. ferroni correction. 200 emails were sent out. 46 responses were excluded from the analysis as non-eligible to participate. 38 did Ethical considerations not respond. 116 completed the questionnaire in full The study was approved by the institutional board of each (estimated response rate 75.3%). participating patient association (Greek Thalassaemia

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Federation 480/3-12-2018 and Panhellenic Association for of the inpatient health services they received. All other Patients with Thalassaemia 1/22-11-2018) and was in line health care services had higher scores in this subscale. with the ethical standards of the Declaration of Helsinki. Availability subscale Participation was voluntary, data were anonymized and The lowest availability scores were reported for the trans- informed consent for participation was requested and ob- fusion unit (2, IQR = 1) and inpatient (median 2, IQR = 2) tained from all participants. and outpatient (median 2, IQR = 1) health care services. Results Higher median availability scores were reported for both for the prescription and dispensing of medication (3, IQR Patient characteristics = 1 for both) and laboratory tests (3, IQR = 1). Table 1 shows the characteristics of the respondents: Association between subscale scores and most were women (51.7%), were between 36 and 50 years old (53.4%) and lived in urban areas (82.7%). Over half patient characteristics (69.0%) held a tertiary education degree. Just over 70% Correlations between responses and respondent sociode- had a monthly income of between 501 and 1500 euros (€), mographic characteristics (Table 3) identified low income 36.2% thought that their economic status was bad or very and living in rural areas as the main barriers to access to bad, i.e. they faced financial challenges, and 95.7% were health care services for transfusion-dependent patients. covered by social insurance, while 4.3% received welfare These characteristics were associated with lower scores benefits, which in Greece grant free access to expensive in almost all subscales. pharmaceutical and hospital care. Due to the sufficiency Participants living in rural areas had significantly of coverage, 96.6% did not have a complementary private lower scores in accessibility (Mann–Whitney U = 468.0, insurance plan. P = 0.014), adequacy (U = 490.5, P = 0.036), affordability U 5 As questionnaire = 519.5, P = 0.011), appropriateness (U = 398.0, P = 0.005) and availability (U = 449.0, P = 0.012) compared with those The reliability for each subscale was good. The Cronbach living in urban areas. alpha was 0.858, 0.870, 0.905, 0.908 and 0.918 for the Furthermore, participants with low incomes had subscales of accessibility, adequacy, affordability, appro- 2 statistically lower scores for adequacy (χ 3 = 9.0, P = 0.029) priateness and availability, respectively. Kolmogorov– 2 2 affordability (χ 3= 19.61, P ≤ 0.001) appropriateness (χ 3 Smirnov normality tests were statistically significant for 2 = 17.70, P ≤ 0.001) and availability (χ 3 = 9.14, P = 0.027) all subscales. subscales, the association between the total score of the Table 2 shows the total mean and median scores for 2 accessibility subscale and income (χ 3 = 5.80, P = 0.122) the 5A subscales and the scores per questionnaire item. was statistically significantly. The adequacy subscale had the lowest median score Pairwise comparison indicated that patients with an (14.0, IQR = 6), followed by availability (16.0, IQR = 7) income of € 1001–1500 a month were less satisfied with and appropriateness (16.5, IQR = 6) (Table 2). The highest the adequacy of the services compared with those with median scores were for accessibility (17, IQR = 7) and an income of more than € 1500 (P = 0.028). Moreover, affordability (17, IQR = 8). patients in the lowest income category (€ ≤ 500) had Accessibility subscale significantly lower scores in the appropriateness subscale Overall, respondents were not faced with overwhelming compared with those in the second income category barriers to accessing health care services in relation to (€ 501–1000, P = 0.027) or in the highest income category their transfusion. All items in the accessibility subscale (€ ≥ 1501, P ≤ 0.001). Patients in the highest monthly had a median score equal to 3. income category had statistically significant higher scores in the affordability subscale compared with those Adequacy subscale with a monthly income of ≤ € 500 (P ≤ 0.001), € 501–1000 Inpatient health services were rated as less adequate by (P ≤ 0.001) or € 1001–1500 (P = 0.007). Participants in the responders (median 2, IQR = 2) whereas all other health highest income category also had better overall score in services provided in relation to a transfusion had a medi- the availability subscale compared with those with an an adequacy score of more than 3. income of ≤ € 500 (P = 0.038) or € 501–1000 (P = 0.048). Affordability subscale On the other hand, participants who self-evaluated their financial situation as very bad/bad scored higher Outpatient health care services and laboratory tests in re- on the affordability subscale than those who evaluated lation to transfusions were a substantial financial burden their financial situation as very good/good or average; on patients and their families (median 2, IQR = 1). High- this difference was marginally statistically significant er median scores were reported for all other items of the (χ2 = 5.66, P = 0.059). subscale. 2 Appropriateness subscale Discussion Inpatient health care services also ranked low in the ap- We investigated barriers that patients with beta-thal- propriateness subscale (median 2, IQR = 1), indicating assaemia in Greece may face in accessing the care they that participants were concerned about the suitability require as well as associations between socioeconomic

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Table 1 Sociodemographic and economic characteristics of the sample Characteristic No. (%) Sex Male 56 (48.3) Female 60 (51.7) Age group (years) 26–35 10 (8.6) 36–50 62 (53.4) 51– 65 39 (33.6) ≥ 66 5 (4.3) Residence Rural 19 (17.3) Urban 91 (82.7) Education Basic 13 (11.2) Secondary 23 (19.8) Tertiary 80 (69.0) Marital status Single 40 (34.5) Married/Cohabitating 60 (51.7) Divorced 16 (13.8) Health insurance status Uninsured/Welfare 5 (4.3) Insured 111 (95.7) Private insurance No 4 (0.4) Yes 112 (96.6) Monthly income (€) ≤ 500 16 (14.2) 501–1000 42 (37.2) 1.001–1500 39 (34.5) ≥ 1501 16 (14.2) Source of income Salary/Salary with overtime payments 35 (31.3) Self-employed 11 (9.8) Pension 66 (58.9) Self-evaluation of financial status Very good/Good 25 (21.6) Fair 49 (42.2) Bad/Very bad 42 (36.2) Profession Agricultural, fishery worker 1 (0.9) Service worker 4 (3.7) Shop and market sales worker 4 (3.7) Clerk 22 (20.2) Administrative, executive or managerial worker 2 (1.8) Scientist, self-employed, technical assistant 21 (19.3) Not working or seeking work for first time 55 (50.5) factors and access to care. Correlations between respons- transportation to having to use three different means es and respondent characteristics identified low income of travel to access the centre. However, accessing and living in rural areas as the main barriers to access. outpatient services seems to be harder for more patients, Respondents with these characteristics scored lower in who stated that they incurred additional costs to access almost all questionnaire subscales. private physicians, particularly out of hours. Barriers to Our findings confirm that respondents are not accessing pharmaceutical care comes mostly from the faced with overwhelming barriers when accessing the fact that in Greece, all medications for an associated transfusion centre or the hospital. However, responses condition have to be prescribed by a specialist outside the range from being extremely close to home or public transfusion unit and this results in additional expense

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Table 2 Scores for the 5 As items Item Mean (SD) Median (IQR) Accessibility total score 16.05 (4.34) 17.00 (7.00) How accessible is the transfusion service that you are receiving treated at? 3.02 (0.78) 3.00 (1.00) How accessible are any general outpatient health services you may be receiving in relation to a 2.47 (0.73) 3.00 (1.00) transfusion? How accessible are general inpatient health services you may be receiving in relation to a 2.40 (1.05) 3.00 (1.00) transfusion? How accessible are medications (prescription) you may be receiving in relation to a transfusion? 2.58 (1.16) 3.00 (1.00) How accessible are medications (dispensing) you may be receiving in relation to a transfusion? 2.78 (0.91) 3.00 (1.00) How accessible are laboratory tests you may be having in relation to a transfusion? 2.70 (0.93) 3.00 (1.00) Adequacy total score 14.73 (4.98) 14.00 (6.00) How adequate is the care you receive in the transfusion unit you are being treated at? 2.43 (1.13) 3.00 (2.00) How adequate are general outpatient health services you may be receiving in relation to a 2.40 (0.96) 3.00 (1.00) transfusion? How adequate are general inpatient health services you may be receiving in relation to a 2.10 (1.15) 2.00 (2.00) transfusion? How adequate are medications (prescription) you may be receiving in relation to a transfusion? 2.65 (1.10) 3.00 (1.00) How adequate are medications (dispensing) you may be receiving in relation to a transfusion? 2.78 (0.93) 3.00 (1.00) How adequate are laboratory tests you may be having in relation to a transfusion? 2.50 (1.09) 3.00 (1.00) Affordability total score 15.92 (5.46) 17.00 (8.00) How affordable is the care you receive in the transfusion unit you are being treated at? 3.14 (1.00) 3.00 (1.00) How affordable are general outpatient health services you may be receiving in relation to a 2.09 (1.02) 2.00 (1.00) transfusion? How affordable are general inpatient health services you may be receiving in relation to a 2.97 (1.12) 3.00 (1.00) transfusion? How affordable are medications (prescription) you may be receiving in relation to a transfusion? 2.74 (1.15) 3.00 (2.00) How affordable are medications (dispensing) you may be receiving in relation to a transfusion? 2.65 (1.10) 3.00 (1.00) How affordable are laboratory tests you may be having in relation to a transfusion? 2.26 (1.08) 2.00 (1.00) Appropriateness total score 15.82 (4.40) 16.50 (5.75) How appropriate do you feel the care is that you receive in the transfusion unit you are being 2.54 (0.94) 3.00 (1.00) treated at? How appropriate are general outpatient health services you may be receiving in relation to a 2.61 (0.80) 3.00 (1.00) transfusion? How appropriate are inpatient general health services you may be receiving in relation to a 2.31 (1.08) 2.00 (1.00) transfusion? How appropriate are the medications (prescription) you may be receiving in relation to a 2.68 (0.98) 3.00 (1.00) transfusion? How appropriate are medications (dispensing) you may be receiving in relation to a transfusion? 2.90 (0.85) 3.00 (0.30) How appropriate are laboratory tests you may be having in relation to a transfusion? 2.46 (0.96) 3.00 (1.00) Availability total score 15.06 (5.11) 16.00 (7.00) How available to you is the care you receive in the transfusion unit you are being treated at? 2.45 (1.11) 2.00 (1.00) How available to you are general outpatient health services you may be receiving in relation to a 2.32 (1.00) 2.00 (1.00) transfusion? How available to you are general inpatient health services you may be receiving in relation to a 2.23 (1.07) 2.00 (2.00) transfusion? How available to you are medications (prescription) you may be receiving in relation to a 2.53 (1.06) 3.00 (1.00) transfusion? How available to you are medications (dispensing) you may be receiving in relation to a 2.73 (0.96) 3.00 (1.00) transfusion? How available to you are laboratory tests you may be having in relation to a transfusion? 2.55 (0.99) 3.00 (1.00)

SD: standard deviation; IQR: interquartile range and time. Respondents were also faced with challenges The situation is somewhat different when it comes in accessing laboratory test services and were required to adequacy of services in the transfusion centre. to carefully plan the day and time of their visit to ensure Responders considered the care they receive somewhat access. adequate; most of the concerns centred around the

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Table 3 Associations between participant characteristics and subscale total scores Subscale Median (IQR) P-value Accessibility Sex Female 17.00 (7.00) 0.564 Male 17.00 (6.00) Residence Rural 13.00 (6.00) 0.014 Urban 17.00 (6.00) Education Basic 14.50 (7.25) 0.215 Secondary 17.00 (5.00) Tertiary 17.50 (7.00) Age group (years) 26-35­ 13.50 (6.75) 0.450 36-­50 17.00 (7.00) ≥ 51 17.00 (6.25) Marital status Single 18.00 (7.50) 0.548 Married/Cohabiting 17.00 (6.00) Divorced 15.00 (6.00) Income (€) ≤ 500 14.50 (6.00) 0.122 501–1000 16.50 (5.25) 1001–1500 15.00 (6.00) ≥ 1501 18.50 (4.00) Self-evaluation of financial status Very good/Good 17.00 (7.00) 0.725 Average 16.00 (7.75) Very bad/Bad 17.00 (6.00) Adequacy Sex Female 14.00 (6.25) 0.595 Male 14.00 (6.00) Place of residence Rural 12.00 (6.00) 0.036 Urban 15.00 (6.50) Education Basic 14.00 (11.00) 0.802 Secondary 14.00 (6.00) Tertiary 14.50 (6.75) Age group (years) 26–35 12.00 (7.50) 0.224 36–50 14.00 (7.00) ≥ 51 15.00 (6.00) Marital status Single 16.00 (8.00) 0.555 Married/Cohabiting 14.00 (6.00) Divorced 13.00 (7.00)

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Table 3 Associations between participant characteristics and subscale total scores (continued) Subscale Median (IQR) P-value Income (€) ≤ 500 14.00 (10.00) 0.029 501–1000 14.50 (6.75) 1001–1500 12.50 (7.00) ≥ 1501 17.00 (5.75) Self-evaluation of financial status Very good/Good 14.00 (7.50) 0.549 Average 13.00 (7.00) Very bad/Bad 15.00 (6.00) Affordability Sex Female 17.00 (5.50) 0.666 Male 17.00 (8.00) Place of residence Rural 12.00 (9.00) 0.011 Urban 18.00 (6.00) Education Basic 12.00 (12.00) 0.175 Secondary 18.00 (8.00) Tertiary 17.00 (6.00) Age group (years) 26–35 18.00 (14.5) 0.754 36–50 17.00 (7.00) ≥ 51 17.00 (8.00) Marital status Single 18.00 (11.50) 0.670 Married/Cohabiting 17.00 (7.00) Divorced 17.00 (5.00) Income (€) ≤ 500 14.50 (11.25) ≤ 0.001 501–1.000 15.00 (7.75) 1001–1500 17.00 (5.00) ≥ 1501 20.00 (2.75) Self-evaluation of financial status Very good/Good 17.50 (6.25) 0.059 Average 16.50 (8.50) Very bad/Bad 18.00 (7.50) Appropriateness Sex Female 16.00 (5.00) 0.381 Male 18.00 (6.00) Residence Rural 13.00 (8.00) 0.005 Urban 17.00 (5.25) Educational level Basic 14.00 (5.50) 0.558 Secondary 17.00 (6.00) Tertiary 16.50 (5.00)

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Table 3 Associations between participant characteristics and subscale total scores (concluded) Subscale Median (IQR) P-value Age group (years) 26–35 15.00 (8.50) 0.658 36–50 16.00 (5.00) ≥ 51 17.00 (6.00) Marital status Single 17.00 (5.00) 0.792 Married/Cohabiting 16.00 (6.00) Divorced 16.00 (6.00) Income (€) ≤ 500 12.00 (7.00) ≤ 0.001 501–1000 18.00 (6.00) 1001–1500 16.00 (5.50) ≥ 1501 19.00 (5.00) Self-evaluation of financial status Very good/Good 15.00 (5.50) 0.328 Average 16.00 (6.75) Very bad/Bad 18.00 (5.00) Availability Sex Female 15.00 (6.75) 0.890 Male 16.00 (7.75) Residence Rural 12.00 (10.00) 0.012 Urban 16.00 (6.00) Education Basic 14.50 (9.50) 0.425 Secondary 16.00 (5.00) Tertiary 15.00 (7.00) Age group (years) 26–35 12.00 (9.00) 0.394 36–50 15.00 (6.00) ≥ 51 16.00 (8.50) Marital status Single 15.50 (7.00) 0.693 Married/Cohabiting 15.50 (6.25) Divorced 16.50 (7.50) Income (€) ≤ 500 14.00 (9.00) 0.027 501–1000 15.00 (7.00) 1001–1500 15.00 (4.50) ≥ 1501 18.50 (4.50) Self-evaluation of financial status Very good/Good 15.00 (7.50) 0.694 Average 16.00 (7.00) Very bad/Bad 16.00 (7.50)

IQR = interquartile range.

1489 Research article EMHJ – Vol. 26 No. 12 – 2020 condition of the blood they receive (particularly if it is tests more available. fresh or not). Adequacy scores of outpatient and inpatient While data are limited on access to treatment among care were similar. Most problems came from the fact thalassaemia patients in Greece, our findings confirm that patients had to carefully plan the time and date of a previous qualitative survey that highlighted barriers their visit. On the other hand, pharmaceutical care was in access to pharmaceutical care and diagnostic tests, considered more adequate. Once a prescription is issued, primarily due to cost (25). patients feel that they receive adequate care at the point Our findings are also in accordance with previous of dispensing. studies on barriers in access to health care for other Access is also largely free at the point of delivery. This chronic diseases, such as rheumatoid arthritis (14), is especially true in the transfusion centre and inpatient multiple sclerosis (15) and cancer (16), which identified hospital services, although not as much when it comes socioeconomic status and distance from urban centres to outpatient and laboratory test services, which was as key contributors to barriers to access. Inequalities in reflected on total affordability scores. Equally, even health care were also reported among vulnerable patient though all thalassaemia-related therapies in Greece are subgroups, such as intravenous drug users (17). dispensed at a 0% copayment rate, patients thought that accessing pharmaceutical care placed a disproportionate To our knowledge, this is the first study that assesses burden on their or their family’s finances. levels of and barriers to access to health care services among patients with transfusion-dependent beta- Despite their long-standing relationship with their thalassemia in Greece and elsewhere. Our study was physicians and staff at the transfusion centre, patients conducted by email, therefore, patients with no registered still felt that the care they receive might not be appropriate email with their patient association could not participate. and looked for additional information or services This may have introduced sampling bias as it is likely elsewhere. In addition, the scores for the appropriateness that elderly patients with no access to the Internet or no of inpatient hospital services were low. This possibly computer skills were not able to participate. comes from the fear that patients are under-transfused because of blood shortages, which is a serious challenge The limited literature on the unmet needs of patients affecting blood transfusions in Greece (20). Patients with thalassaemia in Greece may indicate that the appear to be happier with outpatient services. This may widespread availability of oral chelators has reduced the be largely explained by the fact that they can select their pressure on payers, providers and patients to further own outpatient care provider, most of the times at a fee advance treatment. Current treatment options are mainly paid out of pocket, so they have greater freedom of choice. limited to blood transfusion and oral chelation. Research Equally, responders considered their pharmaceutical care is needed on new treatment pathways, including possibly appropriate to a lesser or greater extent. new treatments, to minimize transfusion burden in the Responses to the composite measure of availability are first place. important as they may be used to cross-validate responses As advances in the management of beta-thalassaemia to other sections of the survey. Lower availability scores are being made, it is important to understand, map and in the transfusion centres and in inpatient and outpatient agree on the transfusion burden of patients with beta- services were mostly due to the long waiting times and thalassaemia in Greece and elsewhere to realign health the need for careful planning to access those services. policies to deliver measurable improvement in the lives Respondents found pharmaceutical care and laboratory of patients.

Acknowledgement We thank the the Greek Thalassaemia Federation and the Panhellenic Association for Patients with Thalassaemia that re- sponded to our call for this research and particularly their members, who shared their perspective and experience with us. Funding: This work was supported by an unrestricted research grant from the biopharmaceutical company, Celgene (grant number: 3422389/11.04.2018). The funding body had no role in the design of the study, data collection and analysis, interpretation of the data and in writing the manuscript. Competing interests: None declared.

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Accès aux soins de santé pour les patients thalassémiques en Grèce : étude transversale Résumé Contexte : La prévalence et la charge clinique de la bêta-thalassémie en Grèce sont élevées. Peu d’informations sont disponibles sur les besoins non satisfaits des patients atteints de bêta-thalassémie et les obstacles à l’accès aux soins. Objectifs : La présente étude avait pour objectif d’examiner les obstacles auxquels les patients grecs atteints de bêta- thalassémie dépendante des transfusions sont confrontés lors de l’accès aux soins, ainsi que les associations entre les facteurs socio-économiques et l'accès aux soins. Méthodes : Une étude transversale a été menée entre novembre 2018 et janvier 2019. L’échantillon comprenait 116 patients atteints de bêta-thalassémie membres des deux associations de patients panhelléniques pour les personnes atteintes de thalassémie. Tous les répondants étaient dépendants des transfusions. L’enquête a personnalisé et utilisé l’outil Patient Access Partnership 5As of access pour mesurer l’accès des participants aux services de soins de santé (sous- échelles : accessibilité, adéquation, accessibilité économique, pertinence et disponibilité). Des données sur leurs caractéristiques socio-économiques ont également été enregistrées. Le lien entre le score total à chaque sous-échelle et les caractéristiques des patients a été examiné à l'aide des tests de Mann-Whitney ou de Kruskal-Wallis. Résultats : Les répondants considéraient que les services de soins hospitaliers étaient moins adéquats et appropriés et que les services ambulatoires et les analyses en laboratoire étaient plus coûteux. Les services ambulatoires sont également perçus comme moins disponibles. Le revenu des participants était significativement associé à toutes les sous- échelles sauf l’accessibilité, et la vie en milieu rural était fortement liée aux cinq sous-échelles. Conclusions : Les obstacles à l’accès aux soins de santé parmi les patients atteints de bêta-thalassémie qui reçoivent des transfusions persistent, en particulier pour ceux qui vivent loin des centres de transfusion et ont des revenus plus faibles. Il est important de comprendre et de recenser les besoins médicaux et sociaux non satisfaits des patients atteints de bêta-thalassémie en Grèce au moment de l’étude, afin de concevoir et de mettre en œuvre une politique de santé ciblée permettant d’améliorer sensiblement la vie des patients.

إتاحة الرعاية الصحية ملرىض أنيميا البحر األبيض املتوسط )الثالسيميا( يف اليونان: دراسة مقطعية كريياكوس سوليوتيس، كريستينا جولنا، صوفيا نيكواليدي، جورجيا فاثيا، ستانيمري هاسوردجييف اخلالصة إناخللفية: معدل انتشار والعبء الرسيري لبيتا-ثالسيميا باليونان مرتفعان. وال يتوافر سوى ٍقدر ٍضئيل من املعلومات حول االحتياجات غري امللباة ملرىض البيتا-ثالسيميا والعقبات التي حتول دون حصوهلم عىل الرعاية. األهداف:هدفت هذه الدراسة إىل دراسة العقبات التي يواجهها مرىض البيتا-ثالسيميا التي تعتمد عىل نقل الدم يف اليونان عند احلصول عىل الرعاية، وأوجه الصلة التي تربط بني العوامل االجتامعية االقتصادية واحلصول عىل الرعاية. طرق البحث: ُأ َت جريدراسة مقطعية يف الفرتة بني نوفمرب/ترشين الثاين 2018ويناير/كانون الثاين 2019. وشملت العينة 116 ًمريضا بالبيتا- ثالسيميامن أعضاء اثنتني من مجعيات الشعوب اليونانية ملرىض الثالسيميا. وكان مجيع املستجيبني من مرىض بيتا-ثالسيميا التي تعتمد عىل نقل " " الدم. وقد ُوضع املسح بمواصفات خاصة واستخدم املقاييس اخلمسة التي وضعتها رشاكة حصول املرىض عىل الرعاية لقياس مدى حصول املشاركني عىل خدمات الرعاية الصحية )املقاييس الفرعية: اإلتاحة، والكفاية، والقدرة عىل حتمل التكاليف، واملالءمة والتوافر(. ُوسجلت ًأيضا بيانات عن خصائصهم االجتامعية االقتصادية. ُوفحصت الصلة بني الدرجة اإلمجالية لكل مقياس فرعي وخصائص املريض باستخدام اختباري مان ويتني وكروسكال واليس. النتائج: رأى املستجيبون أن اخلدمات ُامل ّ مة قدللمرىض الداخليني أقل من حيث الكفاية واملالءمة، كام أن اخلدمات والفحوص ُاملختربية للمرىض اخلارجيني أقل من حيث القدرة عىل حتمل نفقاهتا. ُونظر ًإىل أيضاخدمات املرىض اخلارجيني عىل أهنا أقل ً. توافراوارتبط دخل املشاركني ًارتباطا ًكبريامن الناحية اإلحصائية بجميع املقاييس الفرعية، ما عدا اإلتاحة، كام ارتبطت اإلقامة يف املناطق الريفية ً ارتباطا ًكبريا بجميع املقاييس الفرعية اخلمسة. ال االستنتاجات:يزال هناك عقبات حتول دون حصول مرىض البيتا-ثالسيميا عىل خدمات نقل الدم، خاصة بالنسبة للذين يعيشون ًبعيدا عن مراكز نقل الدم ولدهيم دخل أقل. ومن املهم َهم فاالحتياجات الطبية واالجتامعية احلالية غري امللباة ملرىض البيتا-ثالسيميا يف اليونان وحتديدها لتصميم وتنفيذ سياسة صحية مستهدفة يمكنها أن ُحت ّ ن سحياة املرىض عىل نحو يمكن قياسه.

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Factors that motivate and hinder blood dona- tion in Greece. Transfus Med. 2007;17(6):443–50. https://doi.org/10.1111/j.1365-3148.2007.00797.x 21. Hauk L. Severe blood shortages reinforce the importance of reducing wastage. AORN J. 2018;107(5):P4. https://doi.org/10.1002/ aorn.12160 22. Souliotis K, Peppou L, Agapidaki E, Tzavara C. Health democracy index: development and validation of a self-reported instru- ment for measuring patient participation in health policy. Front Public Health. 2018;6. https://doi.org/10.3389/fpubh.2018.00194 23. Lepkowski J. Sampling the difficult-to-sample. J Nutr. 1991;121(3):416–23. https://doi.org/10.1093/jn/121.3.416 24. Souliotis K, Hasardzhiev S, Agapidaki E. A conceptual framework of mapping access to health care across EU Countries: the Patient Access Initiative. Public Health Genomics. 2016;19(3):153–9. https://doi.org/10.1159/000446533 25. Economou C. 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Factors affecting hookah among females in the Islamic Republic of Iran: a qualitative study

Mohammad Bazrafshan,1 Amir Mansouri,2 Hamed Delam,3 Behnam Masmouei 4 and Nasrin Shokrpour 5

1Department of Nursing, School of Nursing, Larestan University of Medical Sciences, Larestan, Islamic Republic of Iran. 2Department of Paramedi- cal School, Gerash University of Medical Sciences, Gerash, Islamic Republic of Iran. 3Student Research Committee, Larestan University of Medical Sciences, Larestan, Islamic Republic of Iran. 4School of Nursing Hazrat Zahra (P.B.U.H) Abadeh, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 5Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. (Correspondence to: Mohammad-Rafi Bazrafshan: m.bazraf- [email protected]).

Abstract Background: The prevalence of hookah smoking in the Islamic Republic of Iran is increasing among females, especially in the southern cities. Aims: The aim of this study was to investigate the factors influencing hookah tobacco smoking among females in the Islamic Republic of Iran. Methods: In this qualitative study, 52 females who use hookah were selected (25–71 years old) from the cities of Evaz and Gerash and were interviewed. The participants were selected using purposive sampling and the data were gathered using semi-structured interviews. Data analysis was performed using the conventional approach of qualitative content analysis. Results: Most participants were aged between 25 and 35 years old and 55.8% were married. Three main themes were iden- tified from the qualitative data including: personal factors, family factors and social factors. Conclusions: The findings of this study indicate that the reasons for hookah smoking were based on complex interac- tions between individual, family, and social factors. In order to successfully reduce hookah smoking in females it is neces- sary to consider an approach that uses these social factors. Keywords: Smoking, hookah, qualitative research, addiction, Iran Citation: Bazrafshan M; Mansouri A; Delam H; Masmouei B; Shokrpour N. Factors affecting hookah tobacco smoking among females in the Islamic Republic of Iran: a qualitative study. East Mediterr Health J. 2020;26(12):1493–1501. https://doi.org/10.26719/emhj.20.140 Received: 28/01/20; accepted: 13/05/20 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Background few studies conducted on hookah smoking among males and females, and were primarily quantitative rather than Tobacco use is one of the leading causes of death, illness qualitative (11-13). and poverty globally. It has been estimated that there are more than 1.3 billion smokers worldwide, of which 82% In a study conducted by Baheiraei et al. four main live in low- and middle-income countries (1). There are themes were extracted from the qualitative data, various types of tobacco products such as cigarettes, ci- including positive attitudes towards hookah smoking, gars, bidi, pipes and hookah (2). Much attention has been social and family facilitators, and psychosocial needs (14). focused on cigarette smoking but many people, especially In a study by Sakineh Dadipoor (15) the themes of climate- in low- and middle-income regions, smoke tobacco using related association or erroneous beliefs was deduced. hookah (3). Known as ‘ghalyan’ in the Islamic Republic of Thus, a variety of themes have been extracted from a Iran (4), hookah has a historical and cultural origin (5,6). number of qualitative studies attempting to examine the Studies have shown that hookah is more socially accept- causes of women’s tendency to smoke tobacco, especially able than cigarette smoking and is considered less harm- hookah. Due to the high rate of tobacco use and its health ful and addictive (7). risks and the apparent importance of hookah smoking Using tobacco has increased among females of among females, a qualitative study was deemed to be the whom many are unaware of the gender-specific health best approach to research this area. risks associated with tobacco use including cervical Methods cancer, osteoporosis, poor pregnancy outcomes, and early menopause (8,9). In the Islamic Republic of Iran In this study a qualitative content analysis approach with one of the health and social concerns is the increasing a conventional qualitative content analysis method was consumption of hookah smoking among females. The used. Coded classes were extracted directly and induc- results of the National Survey of Risk Factors of Non- tively from the raw data without formatting the precon- Communicable Diseases in showed that more than half ceived categories or theoretical views (16). The samples in of female tobacco smokers used hookah (10). Currently, this study were female current hookah smokers. Inclu- most tobacco smoking studies in the Islamic Republic sion criteria were the subjects’ willingness to participate of Iran have focused on cigarette smoking, with only a in the study, residents of the cities of Evaz and Gerash,

1493 Research article EMHJ – Vol. 26 No. 12 – 2020 familiarity with the Farsi language, and ability to share Table 1 Participants’ characteristics their experiences about the reasons for hookah smoking. Variable Number % Participants were excluded if they were reluctant to con- Age (years) tinue participation in the study. 25-35 15 28.8 The method of data collection was the use of semi- structured interviews between July and September 2019. 36-45 13 25.0 Interviews began with an explanation of the purpose of 46-55 11 21.2 the research for the participants, followed by the general 56-65 9 17.3 open-ended question, “Can you talk about your first 66-75 4 7.7 experience of hookah smoking?” This was followed by Level of education more focused questions on specific issues. If needed, Illiterate 8 15.4 the researcher used exploratory questions such as, “Can you explain more?” or “Can you give an example?” The Elementary school 9 17.3 form and order of the questions were flexible in response High school 11 21.2 to participants’ replies. At the end of each interview, Diploma 16 30.7 the interviewer asked the participants to discuss other Academic 8 15.4 important issues that were not addressed during the Marital status interview. The time and place of the interview were determined after completing the consent form. With the Single 23 44.2 consent of the participants, audio recordings and field Married 29 55.8 notes were used to enhance the accuracy of the data collection. Interviews were conducted with a researcher. The mean duration of each interview for participants 35-year-old woman said, “my aunt had great presence was approximately 45 minutes. The data collection was when she smoked a hookah and command over others. I finalized after researchers reached saturation. After 47 like to be like my aunt”. interviews were conducted, further interviews did not Believing hookah smoking to be harmless, and even have any extra information to offer. to have healing effects. A 57-year-old woman said, “Many To analyze the data, researchers first recorded each people smoked hookah and lived to 70 and 80 years and more. interview followed by verbatim transcription that was Even our elderly drank water from the vase of hookah for entered into MAXQDA 10 software. Each text was broken abdominal pain or they rub its ashes into the throat of a person down into meaning units, which were grouped together. with a cold”. Finally, based on the content and similarities, the main Dependence on hookah smoking. A 42-year-old classes were formed using subcategories. Lincoln woman said, “I just know that if I don’t smoke, I have a bad and Guba’s criteria (2007) were used to improve the mood, and I feel better when I smoke”. accuracy and rigour of the findings 17( ). After extensive Individuality and attention-seeking were also reasons processing of data collection and analysis, a selection for smoking hookah. A 39-year-old woman said, “I would of representative samples were checked for accuracy by like to show off. Hookah is one way to show that I’m fearless”. qualitative research experts, and the initial codes were checked by contributors to increase the credibility of the Curiosity and seeking new experiences. A 47-year-old data in this study. woman said, “It was interesting for me to experience hookah”. Craving during pregnancy. A 41-year-old woman said, Ethical considerations “I had pica during my pregnancy. I found smoking hookah This study was approved by Larestan University of calmed me down. Gradually I became a hookah smoker”. Medical Sciences Ethics Committee (IR.LARUMS. Lack of negative attitudes toward hookah. A 26-year- REC.1398.012). old woman said, “Hookah didn’t affect my health and Results appearance”. Reducing discomfort and pain. A 40-year-old woman Fifty-two interviews were undertaken with female hook- said, “When I’m worried I smoking hookah to give me peace”. ah smokers, mean age was 44.53 ± 12.86 years. Through data analysis, 39 subcategories and 3 main categories in- Rebellion and feminist sympathies. A 45-year-old cluding personal factors, family factors, and social factors woman said, “Why can men do anything but women cannot? were extracted from the data. They use hookah and do other things. At least I can smoke hookah”. Personal factors The aspects of fun and pleasure of hookah smoking Some participants considered the imitation of other peo- were another factor factors. A 28-year-old woman said: ple an effective draw to hookah smoking. A 58-year-old “When I smoke a hookah, it gives me pleasure and joy. woman said, “Others smoke hookah, I also smoke hookah”. Hookah really entertains me and it is a pleasure means Some participants considered following others as for me”. role-models an effective draw to smoking hookah. A A feeling of loneliness was one of the personal factors.

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Table 2 Summary of study findings Themes Subthemes Personal factors Imitation - role-modeling - believing hookah smoking to be harmless - dependence on hookah smoking - exhibitionism - curiosity - craving during pregnancy - positive attitude towards hookah – relaxation and discomfort alleviation - rebellion - pleasure - loneliness - temptation - mental illness - preferring flavoured tobacco - being single and higher age of marriage - Illiteracy and low education level Family factors Marital problems - family conflicts - responsibility for the preparation of hookah - pretext for family gatherings and meeting friends - strict household smoking restrictions - Lack of adequate control and awareness from the family - hookah smoking by family members - gender bias Social factors Hookah as a household item - traditional view of the role of women in society - easy access to hookah paraphernalia - availability of online hookah stores - existence of places for hookah smoking - lack of appropriate recreational facilities for women - poverty - Lack of attention to anti-smoking laws - affordable hookah prices - possibility of hookah smoking in public places – approval of hookah smoking among women - hookah smoking as a form of social protection for women - Impact of media - peer pressure

A 64-year-old woman said: “My husband has gone to work about them”. in the Gulf countries. I am alone. The hookah is a friend for me”. Hookah smoking by family members. A 49-year-old The temptation for hookah smoking in the encounter woman said, “Both my parents smoke hookah. Well, like them, with hookah smokers was one of the personal factors. A I started smoking hookah”. 48-year-old woman said:” when I am in a group of people who Gender-bias. A 66-year-old woman said, “My parents smoke hookah I also like to do so. I cannot control it”. just wanted to put the girls into housekeeping. Hookah smoking Having a mental illness. A 49-year-old woman said, was a kind of protest against this discrimination”. “The doctor said I am depressed, I think hookah makes me feel better”. Social factors Preferring flavoured tobacco. A 29-year-old woman The traditional view of the role of women. A 31-year-old said, “There is flavoured tobacco that most young people prefer woman said, “Women in small towns often have to stay at to use. It is attractive”. home. I’m bored at home. My fun is hookah”. Being single and later age of marriage. A 44-year-old The availability of hookah as a household item. A woman said, “A married woman is busy with home life but I do 59-year-old woman said, “There is at least one hookah in every not have these concerns. For me, hookah smoking is a pretext to home, if they have guests, they serve them hookah”. being in a family”. Accessibility and ease of purchase of hookah. A From past to now, it was easy to buy Belief that they can quit hookah smoking. A 33-year- 71-year-old woman said, “ hookah and tobacco”. old woman said, “Hookah does not cause addiction. Little effort is needed to quit smoking hookah”. Some coffee shops or traditional restaurants offer hookah. A 40-years-old woman said, “hookah is essential Low education level. A 46-year-old woman said, in tea and coffee houses”. “Illiteracy makes us not understand what doctors and books say about the dangers of hookah”. Availability of online hookah stores. A 28-year-old woman said, “You can just go to an online store and order Family factors hookah”. Marital problems and family conflicts. A 31-year-old The lack of appropriate recreational facilities for woman said, “I have problems with my husband. I smoke women in the city. A 43-year-old woman said, “The city is hookah to keep calm”. A 30-year-old woman said, “I have a small. There is no appropriate place for women to have fun”. disagreement with my husband, so I smoke hookah”. Poverty. A 36-year-old woman said, “I do not have a Responsibility for the preparation of the hookah. A wealthy family. The price of the ticket for the swimming pool is 55-year-old woman said: “I remember I was responsible for high, but hookah is inexpensive”. preparing hookah. I gradually became a hookah smoker”. The freedom to smoke hookah publically. A 55-year- Hookah smoking was a pretext for family gatherings old woman said, “Anyone who wants to smoke hookah can do and meeting friends. A 42-year-old woman said, “I think so anywhere, for example, in the park”. hookah can bring people together and keep them friendly”. The lack of attention to laws prohibiting smoking in Strict household smoking restrictions (lack of) were public places. A 53-year-old woman said, “There is a legal instrumental in women smoking hookah. A 28-year- ban on tobacco smoking in workplaces and other public spaces, old woman said, “My father who died was not someone who but it is just a slogan”. seriously prevented me from smoking hookah”. Approval of hookah smoking among females. A Lack of sufficient control and familial awareness. A 46-year-old woman said, “There is no opposition to hookah 50-year-old woman said, “My family thought it was normal. smoking for women”. They didn’t even talk about its dangers. They didn’t even know Believing that hookah smoking by a woman at home

1495 Research article EMHJ – Vol. 26 No. 12 – 2020 would help protect her from exposure to risks outside the In the present study the perception of loneliness was home. A 63-year-old woman said, “It is better for a woman to indicated as a draw to hookah smoking and supported stay at home and smoke hookah instead of going out and engage by other studies that also indicate hookah use is higher in immoral activities”. among single people and widows (29); this finding could The Impact of media on hookah smoking. A 56-year- confirm that loneliness as well as being single can lead to old woman said, “Hookah smoking was shown in movies. We hookah use. Reducing discomfort was another reason for watched these movies and were impressed”. the use of hookah, which has been confirmed in several studies (30,31). The influence of peer groups on hookah smoking. A 25-year-old woman said, “In friends gatherings if they smoke Breaking the norms of gender roles and feminist hookah and offer it to me I have no choice”. tendencies have been cited as one of the reasons for the use of hookah, which equates to equality with men, Discussion but this finding has not been observed in other studies. In addition, one of the reasons for using hookah was Personal domain association with mental illness, which has been confirmed In the findings of this study 17 codes were observed, in various studies (32,33); however, no such finding was which have the highest multiplicity. One participant re- found in Goodwin et al. (34), who found that there was no ported role-modeling in the draw to hookah use. Other significant relationship between hookah use and mental studies have shown that imitating others can trigger or illness and stress, but there was a significant relationship encourage continuing cigar smoking (18,19). However, between cigarette use and mental illness. this finding has not been reported in hookah studies. This Another reason indicated for the increase in the use of difference may be due to the fact that smoking cigars/ hookah is the appeal of flavoured tobacco, which was also cigarettes is easier to do in public whereas hookah is a found in American society (35). This type of tobacco is tool that requires a seated environment. Another finding more popular among women of childbearing age, and if of this study was the use of hookah for self-expression, this category of tobacco is banned then the use of hookah which was also reported by Baheiraei et al. (20), but An- could be reduced (36). One of the reasons found for using barlooi et al. showed that there was a significant relation- hookah in this study was Pica during pregnancy, but was ship between smoking and high school students’ self-es- not found in the Kahr et al. study, which found that women teem, yet this relationship was not indicated for hookah considered cigarettes less dangerous than hookah during smoking (21). However, participants in the present study pregnancy. However, in another study it was observed stated that hookah use is a factor for individuality and that women preferred flavoured tobacco hookah during self-expression; Mahmoodabad et al. (22) indicated that pregnancy such as menthol, believing that it is good for there was a significant relationship between tobacco use, the health of the mother and fetus (37,38). including hookah, and self-esteem and identity. In this study it was found a major reasons for using Family domain hookah was curiosity, which was supported by Gentzke In the family domain 8 subthemes were extracted and et al. (23) whereby 14.6% of people who had never used dominated by the factor of imitation. As shown in the tobacco and 45.9% of those who always use tobacco were Bashirian et al. study, adolescents who have family mem- curious about hookah, and this finding is consistent with bers using hookah are also more likely to use hookah (27). those of the present study. In this study, temptation is In addition, other studies have observed that an impor- also mentioned as one of the reasons for using hookah; tant factor influencing addiction was inhalation of sec- this finding was also indicated in a study by Jeihooni who ond-hand smoke (39). In a study conducted in 2016, more examined the causes of hookah use in students (24). than 20 000 young people in the United States found that Another personal finding of this study on hookah use most people who used hookah frequently lived with an was the lack of a negative view of the effects of hookah addicted hookah smoker (40). use on the body, which may have been due to declining Considering that hookah smoking is frequently seen levels of knowledge and awareness. It was also observed as integral to family and friends gatherings, a qualitative in a study in the United States of America that most study by Baheiraei et al. which looked at the prevalence hookah users did not have a high level of literacy (25). of hookah use in women, supported the current study A study of 270 students in Serbia found that the most finding that hookah preparation was a factor in hookah common reason for students to use hookah was to create smoking addiction. It was also observed that husbands a sense of tranquility (26). This finding was also indicated and wives played an important role in women’s addiction in the present study where participants stated that one to hookah, suggesting that education about the risks of the reasons for using hookah was to induce a feeling should also be aimed at the family level (5). of calm and reduce discomfort and pain. Another study Hookah smoking is also suggested as a cause of family conducted on male high school students stated that the relationship problems, which is in line with the Bhat et reasons for smoking hookah were the need to feel calm al. study (41). However, another study looked at it from a and reduce stress (27), but Grinberg’s study showed that different approach and reported that the observed causes people who use hookah had a greater perception of pain of problems in family and marital relationships due to than non-users, but this was not significant 28( ). hookah smoking is the resultant prevalence of bad breath

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(42). Familial disapproval of smoking cigarettes was also intentions to give it up for health reasons, yet continued observed as a reason for smoking hookah. In this regard, to use it. This underlies the belief that hookah smoking a study reported that disapproval of women smoking was not addictive, but rather its use could reduce anxiety. cigarettes was prevalent in the Iranian population, but This observation is included in the personal domain of less disapproval of smoking hookah, which is consistent the current study. with the results of the present study (43). One finding in the current study remains unique, Other factors influencing the draw to hookah which is the view that hookah smoking can protect smoking among women include reduced supervision women from high-risk behaviours and addiction to more and control by the family. This finding was also observed dangerous substances outside the home. This finding is in the Farideh et al. study, which reported children who consistent with Weina Qu et al. (55), which showed how were of a low socioeconomic and educational level were stress can increase risk taking and aggressive behaviour. more exposed to tobacco smoking (44). The existence of centres outside home for hookah Social domain use was also observed as a contributing factor to hookah addiction among women; in contrast, a study found that In the social domain 13 codes were extracted. A primary hookah use was the most common behaviour within the reason observed for using hookah was the lack of enter- home for users in the United States (40). Another study in tainment for women, which supports studies indicating Iraq found that hookah was mostly used in coffee shops that the draw to smoking hookah in young females was (56) while in the Islamic Republic of Iran, the use of hookah its entertainment and social interaction value (45). These in traditional restaurants is common (57), thus there are findings are in line with the results of the present study cultural dimensions to this phenomenon. Finally, an highlighting the lack of appropriate recreational facili- important reason for using hookah is the power of the ties for women in the social domain (46). In a qualitative media, which has been confirmed in a number of studies, study on 37 Swedish adolescents, reasons for using hook- promoting the use of hookah significantly 58,59( ). ah were meeting friends, being accepted by a group, or using hookah as a criterion for admission into a group. Conclusion Moreover, participants did not have a negative concern- One of the strengths of this study is the qualitative extrac- ing hookah smoking (47), and related studies have indi- tion of various factors shown to influence the behaviour cated that there was a strong link between hookah use and attitudes of women towards hookah smoking. These and having friends who are addicted to hookah or smok- factors were classified into three themes: personal, fami- ing cigarettes (48). ly and social. These factors were considered from several Not viewing hookah smoking as harmful has been perspectives, including childhood and adolescence, such observed in various studies (46,49) as well as ease of as exposure to preparation of hookah at home or having access due to moderate pricing as important reasons for parents smoking hookah, as well as experiencing loneli- addiction (46,50) and the lack of any legal restriction to the ness in adulthood. Despite the psychological contribut- use of hookah (51). Poverty was also found to be a cause ing factors, such as mental illness, physical aspects are for hookah addiction and supported by the Salloum et al. also prevalent such as Pica during pregnancy. Some fac- study (52), which indicated that loack of legal controls tors are also related to the individual, such as curiosity or over access to hookah is a contributing factor to addiction exhibitionism, as well as social ignorance of the harm of (51,53). hookah smoking. The role of society also manifests itself In a qualitative study published in 2019 (54), the in factors such as the lack of appropriate recreational fa- tendency of individuals to use hookah was divided cilities for women, or poverty. Certain factors transcend into three areas: attitude, mental norm, and receiving local or national borders such as the media, while current controlling behaviours. These three areas included 9 legislation fails to exert sufficient control of access to subcategories, and the results of this study showed hookah. that in hookah addiction, people maintained a positive A sense of gender equality has encouraged some attitude towards hookah and consider it harmless when women to take up hookah smoking, while at the same compared to cigarettes, and is considered a suitable time there is an opinion that hookah smoking among substitute. In addition, acceptance in the community and women prevents them from being exposed or tempted availability were mentioned in the social domain, which by inappropriate behaviours beyond the control of the is in line with the findings of the present study. However, family. The reasons are numerous and indicate that the current study differed in the manner of classifying influences behind women taking up hookah smoking are the factors influencing hookah addiction. individual and not necessarily predictable. Qualitative Another study conducted in Fasa in 2015 (24) examined studies such as the present study draw data directly from students’ knowledge and attitudes toward hookah use, women themselves, making it possible to plan and take which observed that more than 80% of students who held appropriate measures on an individual, family and social

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Acknowledgement The authors would also like to thank all the research participants who have contributed to the study. Funding: Faculty of Medical Sciences, Larestan University (1398-003). Competing interests: None declared.

Étude qualitative sur les facteurs influençant le tabagisme par houka chez les femmes en République islamique d’Iran Résumé Contexte : La prévalence du tabagisme par houka en République islamique d’Iran augmente chez les femmes, en particulier dans les villes du sud. Objectifs : l’objectif de la présente étude était d’étudier les facteurs influencant le tabagisme par houka chez les femmes en République islamique d’Iran. Méthodes : Dans cette étude qualitative, 52 femmes sélectionnées qui fumaient la houka (âgées de 25 à 71 ans) dans les villes d’Evaz et de Gerash ont été interrogées. Les participantes ont été sélectionnées sur la base d’un échantillonnage ciblé et les données ont été recueillies dans le cadre d’entretiens semi-structurés. L’analyse des données a été réalisée selon l’approche conventionnelle d’analyse qualitative du contenu. Résultats : La plupart des femmes avaient entre 25 et 35 ans. En termes de statut marital, 55,8% étaient mariées. Trois thèmes principaux ont été identifiés à partir des données qualitatives, à savoir : les facteurs personnels, les facteurs familiaux et les facteurs sociaux. Conclusions : Les résultats de cette étude indiquent que les raisons de l’utilisation de la houka étaient les interactions complexes entre les facteurs individuels, familiaux et sociaux. Pour réussir à réduire le tabagisme par houka chez les femmes, il est nécessaire de tenir compte les facteurs sociaux.

العوامل ّاملؤثرةيف تدخني تبغ الشيشة بني اإلناث يف مجهورية إيران اإلسالمية: دراسة ّنوعية حممد بذرافشان، أمري املنصوري، حامد دالم، هبنام مسموعی، نرسين شكربور اخلالصة اخللفية: يتزايد ّمعدل انتشار تدخني الشيشة يف مجهورية إيران اإلسالمية بني اإلناث، ال ّسيام يف املدن اجلنوبية. األهداف: هدفت هذه الدراسة إىل استقصاء العوامل التي ّتؤثرعىل تدخني تبغ الشيشة بني اإلناث يف مجهورية إيران اإلسالمية. ُ طرق البحث: يف هذه الدراسة ّالنوعية، اختريت 52 امرأة ّ نيدخ الشيشة )يف عمر 25-71 ًعاما( من مدينتي إيفاز وجرياش، وأ َتجري مقابالت معهن. واختريت املشاركات عن طريق أخذ ّعينات هادفة، و ُمجعت البيانات بمقابالت شبه ّمنظمة. ُوح ِّللت البيانات بالنهج التقليدي لتحليل املحتوى النوعي. النتائج:تراوحت أعامر معظم املشاركات بني 25 و35 ًعاما، وكان %55.8 منهن متزوجات. ُوح ّددت ثالثة مواضيع رئيسية من البيانات ّالنوعية اشتملت عىل: العوامل الشخصية، والعوامل العائلية، والعوامل االجتامعية. تشرياالستنتاجات: نتائج الدراسة إىل أن أسباب تدخني الشيشة اعتمد عىل تفاعالت ّمعقدة بني العوامل الفردية واألرسية واالجتامعية. ويستلزم النجاح يف ّاحلدمن تدخني الشيشة لدى اإلناث التفكري يف َن ٍج يستخدم هذه العوامل االجتامعية.

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Eating disorders among Jordanian adolescents with and without dysglycaemia: a comparative study

Huda Al Hourani,1 Rana Ababneh,2 Nahla Khawaja,2 Yousef Khader 3 and Kamel Ajlouni 2

1Department of Clinical Nutrition and Dietetics, Faculty of Applied Health Sciences, The Hashemite University, Zarqa, Jordan. 2National Center for Diabetes, Endocrinology and Genetics, University of Jordan, Amman, Jordan. (Correspondence to: Kamel Ajlouni: [email protected]). 3Department of Public Health. Jordan University of Science and Technology, Irbid, Jordan.

Abstract Background: Studies on eating disorders among Jordanian adolescents have reported variable prevalence rates of 12–40%. Aims: This study aimed to determine the prevalence of eating disorders among Jordanian adolescents with and without dysglycaemia and determine the associated factors. Methods: A comparative cross-sectional study was conducted during the period November 2017–February 2018. The Eat- ing Disorder Diagnostic Scale was used to assess the presence of different types of eating disorders, including anorexia nervosa, bulimia nervosa and binge eating disorder. A typical anorexia nervosa and purging disorder were considered “other eating disorders” in this study. Results: This study included 497 patients with dysglycaemia and 504 age-matched nondysglycaemic participants. Pa- tients with dysglycaemia had a significantly higher prevalence of binge eating disorders compared with nondysglycae- mic participants (11.9% vs 5.8%, P < 0.001). In dysglycaemia group, adolescents who were aged ≥ 14 years were more likely to have bulimia nervosa compared with those < 14 years old. Patients with a sedentary lifestyle were less likely to have bulimia nervosa and binge eating disorders. In the nondysglycaemic group, those aged 14–18 years were more likely to have other eating disorders. Those with dysglycaemia were more likely to have binge eating disorders than those in the nondysglycaemic group (OR = 2.1, 95% CI: 1.3–3.3; P = 0.002) after adjusting for possible confounders. Conclusions: Adolescents with dysglycaemia had higher prevalence of eating disorders compared with their nondysg- lycaemic peers. Screening for eating disorders is recommended among adolescents to secure early detection and subse- quent intervention. Citation: Al Hourani H; Ababneh R; Khawaja N; Khader Y Ajlouni K. Eating disorders among Jordanian adolescents with and without dysglycaemia: a comparative study. East Mediterr Health J. 2020;26(12):1502–1509. https://doi.org/10.26719/emhj.20.86 Received: 03/06/19; accepted: 24/12/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction binging followed by purging to prevent weight gain. In 2013, the DSM also officially recognized binge eating Eating disorders (EDs) are psychiatric conditions charac- disorder (BED) as a distinct eating disorder characterized terized by severe disturbances in eating behaviour that by the ingestion of too much food in a short time (10). result in significant physiologic impairment and, in some cases, increased mortality in some types (1,2). These con- Adolescents with diabetes are at higher risk of eating ditions have significant health effects on people with di- disturbances and consequently of higher rates of disease abetes. Many studies have been conducted to determine complications; EDs among adolescents with TIDM are the association between EDs and type 1 diabetes mellitus associated with poor diabetes control and higher rates (T1DM) and have reported that diabetes is a risk factor of diabetes complications, including ketoacidosis and (3–5). Eating disorders have been shown to be more fre- hospitalization (11). quent in adolescents with diabetes compared with nondi- Studies on EDs among adolescents in the Eastern abetic adolescents (6,7). A 2013 meta-analysis showed that Mediterranean Region are limited in number and also EDs were more common in adolescents with T1DM (7.0%) limited to healthy adolescents. In Egypt, El-Bakry et al. compared with their adolescents with no diabetes (2.8%) reported that 34.7% of adolescent patients with T1DM (8). Previous research has shown that EDs are more than have disordered eating behaviours (12). In Jordan, studies twice as common in young females with T1DM compared on EDs were limited to healthy female adolescents; with their nondiabetic peers (9). these reported variable prevalence rates between 12% The Diagnostic and statistical manual of mental disorders and 40% (13–15). The prevalence of EDs among Jordanian (DSM) specifies a number of diagnoses under “Feeding adolescents with T1DM is unknown; knowing the and eating disorders”, including anorexia nervosa (AN), prevalence is important to help care providers make which is characterized by restriction of energy intake decisions on screening activities and management. relative to requirements, leading to significantly low Therefore, this study aimed to determine the prevalence body weight, and bulimia nervosa (BN), which involves of EDs among Jordanian adolescents with and without

1502 Research article EMHJ – Vol. 26 No. 12 – 2020 dysglycaemia and to determine their associated factors. to prevent weight gain. There were also questions about how much body image problems impact the subject’s Methods relationships and friendships with others. The final Design and participants questions were about the patient’s current weight, height, sex and age. This cross-sectional comparative study included 497 (172 Atypical AN and purging disorder were considered males and 325 females) patients aged 10–24 years with “other EDs”. The Eating Disorder Diagnostic Scale has dysglycaemia (T1DM and pre-DM) who attended the Na- been translated into Arabic and validated by a study done tional Center for Diabetes, Endocrinology and Genetics at the National Center for Diabetes, Endocrinology and and Jordan University Hospital in Amman from Novem- Genetics in 2010 (17). Cronbach’s alpha was 0.80, which is ber 2017 to February 2018, and 504 (175 males and 329 considered acceptable. females) age-matched nondysglycaemic control partici- pants randomly selected from government schools and Anthropometric measures universities. Height was recorded to the nearest 0.5 cm using a stadi- This study was reviewed and approved by the research ometer, with the subject in a standing position and with- ethics committee at the National Center for Diabetes, out shoes. Body weight was recorded to the nearest 0.1 Endocrinology and Genetics. The ethical aspects of the kg using a calibrated scale. The nondysglycaemic partici- present study are covered in the Declaration of Helsinki. pants’ weight and height were measured at their schools Inclusion and exclusion criteria or universities. Body mass index (BMI) was calculated using the standard formula: weight (kg)/height (m)2 and Only adolescents aged 10–24 years were included in this classified into severe thinness, underweight, normal study. The dysglyacemic group included patients diag- weight, overweight and obese. Participants younger than nosed with T1DM or pre-DM. Participants were diag- 19 years of age were classified according to the WHO nosed as having prediabetes if they had impaired fasting growth charts 2007. blood glucose (fasting blood glucose 100–125mg/dL) and/ or impaired glucose tolerance (blood glucose 140–199 mg/ Metabolic control dL 2 hours after a 75-g oral glucose tolerance test). The ex- The choice of treatment for those with T1DM was insu- clusion criteria were: having hypothyroidism, Cushing’s lin plus metformin or insulin alone, whereas pre-DM syndrome, Addison’s disease, growth hormone deficien- patients were treated with metformin. Metabolic control cy, receiving growth hormone therapy and pregnancy. was assessed by HbA1c levels, measured using the Bio- Rad VARIANT II TURBO HbA1 Kit-2.0 (Bio-Rad, Hercules, Sample size c California), which utilizes the principles of ion-exchange The sample size was calculated based on the most recent high-performance liquid chromatography. estimate of ED prevalence rate (14). Assuming that prev- alence of ED is 12%, the minimum sample size needed to Statistical analysis estimate the prevalence within a margin of error of 5% Analyses were conducted using SPSS, version 21.0. Contin- at a level of significance of 5% and power of 80% was uous variables were described using means and standard estimated as 163 in each group. The sample size was in- deviations and categorical variables were described using creased in both groups to have a higher power. percentages. The chi-squared test was used to compare The study tool percentages. Multiple binary logistic regression analysis was conducted to determine factors associated with EDs A questionnaire was designed to collect demograph- and to determine the association between dysglycaemia ic and lifestyle data including age, sex, education level, and EDs. P-value < 0.05 was considered statistically sig- employment, physical activity level, and duration of dys- nificant. glycaemia when present. The diagnostic instrument for EDs was the Eating Disorder Diagnostic Scale, a 22-item Results self-report questionnaire that evaluates the presence of 3 EDs: AN, BN and BED, based on the criteria of the Participants’ characteristics DSM-IV (16). The scale is composed of a combination of The dysglyacemic group included 497 participants (65.4% Likert scores, dichotomous scores and frequency scores. females and 34.6% males) with a mean age of 16.7 years. The questions explored the person’s feelings toward his The nondysglycaemia group included 504 participants or her appearance and having incidents of eating with a (65.3% females and 34.7% males) with a mean age of 16.8 loss of control and how he/she felt after overeating. The years (Table 1). Of those with dysglycaemia, 45.9% had estimated time for completing the questionnaire was 30 T1DM and 54.1% had pre-DM. The mean BMI was higher minutes. in the dysglyacemic group compared with the nondysg- In addition, the questionnaire included questions lycaemia group (25.0 vs 21.2 kg/m2, P < 0.001). Just over a about the person’s experiences of fasting, skipping at least quarter of the dysglycaemia group and around 6% of the

2 meals, making themselves vomit, and using laxatives nondysglycaemia group were obese. The mean HbA1c was or diuretics or being engaged in more intense exercise 8.6% in the dysglycaemia group.

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Table 1 The sociodemographic, clinical, anthropometric, and relevant characteristics of adolescent participants, Jordan, 2017– 2018 Characteristic Dysglycaemia Nondysglycaemia P-value (n = 497) (n = 504) Mean (SD) Mean (SD) Age (years) 16.8 (4.3) 16.8 (4.4) 0.871 Height (cm) 157.4 (12.0) 157.9 (13.1) 0.521 Weight (kg) 63.4 (21.0) 53.6 (13.9) < 0.001 BMI (kg/m2) 25.0 (6.6) 21.2 (4.0) < 0.001 Sex, no. (%) 0.970 Male 172 (34.6) 175 (34.7) Female 325 (65.4) 329 (65.3) BMI category, no. (%) < 0.001 Severe thinness 1 (0.2) 14 (2.8) Underweight 19 (3.8) 44 (8.7) Normal 182 (36.6) 301 (59.7) Overweight 160 (32.2) 116 (23.0) Obese 135 (27.2) 29 (5.8) Physical activity a, no. (%) 0.001 Sedentary 284 (57.1) 234 (46.4) Active 213 (42.9) 270 (53.6)

SD = standard deviation; BMI = body mass index. aPhysical activity was classified according to the International Physical Activity Questionnaire (sedentary: physical activity ≤ 10 continuous minutes per week and up to 150 minutes per week. active: moderate to high activity like walking for ≥ 5 days/week and ≥ 30 minutes per session).

Prevalence of eating disorders mia group, adolescents aged ≥14 years were more likely to have BN compared with those < 14 years old. Age was Those with dysglycaemia showed a higher prevalence of not significantly associated with the other 2 types of ED. BED compared with those who did not have nondysgly- Patients who reported having a sedentary lifestyle were caemia (11.9% vs 5.8%, P < 0.001) (Table 2). However, there less likely to have BN (OR = 0.2, 95% CI: 0.1–0.5; P = 0.001) were no significant differences in the prevalence of BN and BED (OR = 0.4, 95% C: 0.2–0.8; P = 0.005). and other EDs between the 2 groups. In the nondysglycaemic group, participants who were Table 3 shows the prevalence of EDs in both groups aged 14–18 years were 2.6 times more likely to have other according to the participants’ characteristics. For the EDs compared with those < 14 years (P = 0.014). Also in this nondysglycaemia group, BED was significantly more group, a physical activity was not significantly associated prevalent among females and the other EDs were less with the 3 different types of ED. common among those who were 14–18 years old. In A separate analysis (after adjusting for possible the dysglyacemic group, the prevalence was higher confounders) showed that those with dysglycaemia among older adolescents, females, obese patients, the were 2.1 times more likely to have BED than the physically inactive, and patients with pre-DM. Higher nondysglycaemic group (OR = 2.1, 95% CI: 1.3–3.3; P = BMI, sedentary lifestyle, and pre-DM were statistically 0.002). significantly associated with BED. Discussion Multiple regression analysis In this study, we estimated the prevalence of EDs among Table 4 shows the multiple regression analysis of factors dysglycaemic and nondysglycaemic adolescents in Jor- associated with different types of EDs. In the dysglycae- dan. The prevalence of EDs was higher in dysglycaemic

Table 2 Prevalence of different eating disorders among the Jordanian adolescents, 2017–2018 Disorder Dysglycaemia Nondysglycaemia P-value (n = 497) (n = 504) % % Bulimia nervosa 6.6 4.9 0.158 Binge eating disorder 11.9 5.8 < 0.001 Other eating disorder 17.1 13.9 0.094 Any eating disorder 35.7 25.0 < 0.001

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Table 3 Distribution of eating disorders among Jordanian adolescents with dysglycaemia and nondysglycaemia according to demographic characteristics, 2017–2018 Characteristic Dysglycaemia Nondysglycaemia Bulimia Binge eating Other eating Bulimia Binge eating Other eating nervosa disorder disorders nervosa disorder disorders (n = 33) (n = 59) (n = 85) (n = 25) (n = 29) (n = 70) No. (%) No. (%) No. (%) No. (%) No. (%) No. (%) Age (years) < 14 3 (1.8) 13 (7.8) 30 (18.1) 7 (4.2) 8 (4.8) 25 (15.1) 14–18 12 (8.0) 22 (14.7) 19 (12.7) 5 (3.3) 5 (3.3) 10 (6.6) > 18 18 (9.9) 24 (13.3) 36 (19.9) 13 (7.0) 16 (8.6) 35 (18.8) P-value 0.007 0.132 0.204 0.257 0.093 0.005 Sex Male 7 (4.1) 19 (11.0) 23 (13.4) 6 (3.4) 3 (1.7) 18 (10.3) Female 26 (8.0) 40 (12.3) 62 (19.1) 19 (5.8) 26 (7.9) 52 (15.8) P-value 0.094 0.679 0.108 0.248 0.005 0.088 BMI category Severe thinness 0 (0.0) 0 (0.0) 0 (0.0) 1 (7.1) 1 (7.1) 0 (0.0) Underweight 0 (0.0) 1 (5.3) 2 (10.5) 0 (0.0) 1 (2.3) 1 (2.3) Normal 3 (1.6) 18 (9.9) 24 (13.2) 15 (5.0) 15 (5.0) 43 (14.3) Overweight 12 (7.5) 10 (6.3) 32 (20.0) 7 (6.0) 10 (8.6) 22 (19.0) Obese 18 (13.3) 30 (22.2) 27 (20.0) 2 (6.9) 2 (6.9) 4 (13.8) P-value < 0.001 < 0.001 0.342 0.614 0.436 0.045 Physical activity a Sedentary 29 (10.2) 44 (15.5) 52 (18.3) 13 (5.6) 13 (5.6) 36 (15.4) Active 4 (1.9) 15 (7.0) 33 (15.5) 12 (4.4) 16 (5.9) 34 (12.6) P-value < 0.001 0.004 0.409 0.567 0.859 0.366 Type of dysglycaemia T1DM 8 (3.6) 19 (8.3) 40 (17.5) – – – Pre-DM 25 (9.3) 40 (14.9) 45 (16.7) P-value 0.010 0.025 0.810

BMI = body mass index; T1DM = type 1 diabetes mellitus; Pre-DM = pre-diabetes mellitus. aPhysical activity was classified according to the International Physical Activity Questionnaire (sedentary: physical activity ≤ 10 continuous minutes per week and up to 150 minutes per week. active: moderate to high activity like walking for ≥ 5 days/week and ≥ 30 minutes per session). patients compared with nondysglycaemic participants samples ranges from 2% to 5% (22). We found that (35.7% vs 25.0%). The EDs identified in this study included patients with dysglycaemia were 2 times more likely to BN, BED, and other EDs; no cases of AN were identified have BED than the nondysglycaemic group. This finding in either group. The finding of higher prevalence of EDs is consistent with previous research (23). Mannucci et al. among patients with dysglycaemia is consistent with reported that the prevalence of BED was 4.9% in IDDM, the findings of other studies 4,7,18( ). Young et al. reported patients and 2.7% in controls (24). d’Emden et al. reported that the prevalence of EDs in adolescents with T1DM was that 17.7% of Australian adolescents with T1DM had BED greater compared with their nondiabetic counterparts (25). It was also more common in preteens and early (7% vs 2.8%) (8). Jones et al. found that EDs were more teenage girls with T1DM than in nondiabetic girls (3.0% prevalent in females with diabetes (10%) than in nondi- vs 0.3%) (26). Although EDs can affect individuals of all abetic females (4%) (9). Some research has indicated that ages, adolescence represents a peak lifetime period of diabetes is associated with psychosocial difficulties and increased vulnerability for the onset of EDs; BED has 2 worries (19). This might explain the higher prevalence peaks of onset, the first at a mean age of 14 years and the of EDs among those without diabetes, especially adoles- second between 19 and 24 years old (27). The age range for cents and young adults. the current study was 10–24 years, and the mean age was In the current study, the most common eating disorder 16 years, which might explain the reason that BED was seen in the dysglycaemic patients was BED, which is the the most common ED in this group. most common ED worldwide when compared with AN Obesity is known as a risk factor for inappropriate and BN (20,21). The prevalence of BED in community weight control practices, and is therefore a risk factor for

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Table 4 Multiple logistic regression analysis for factors related to bulimia nervosa, binge eating disorder and other eating disorders in Jordanian adolescents with and without dysglycaemia, 2017–2018 Characteristic Bulimia nervosa Binge eating disorder Other eating disorders OR (95% CI) P-value OR (95% CI) P-value OR (95% CI) P-value Dysglycaemic group Age (year) < 14 1.0 1.0 1.0 14–18 4.7 (1.3–17.3) 0.018 2.0 (0.9–4.2) 0.060 1.5 (0.8–2.8) 0.183 > 18 5.9 (1.7 –20.5) 0.005 1.8 (0.8–3.6) 0.122 0.9 (0.6–1.5) 0.673 Physical activity Active 1.0 1.0 1.0 Sedentary 0.2 (0.1–0.4) 0.001 0.4 (0.2–0.8) 0.005 1.2 (0.8–2.0) 0.413 Non-dysglycaemic group Age (years) < 14 1.0 1.0 1.0 14–18 0.7 (0.2–2.4) 0.625 0.9 (0.2–2.2) 0.522 2.6 (1.2–5.8) 0.014 > 18 1.6 (0.6–4.3) 0.310 1.9 (0.9–4.6) 0.155 0.8 (0.4–1.4) 0.458 Physical activity Active 1.0 1.0 1.0 Sedentary 0.8 (0.4–1.9) 0.640 1.1 (0.5–2.4) 0.751 1.3 (0.8–2.2) 0.321

ED. The EDs that have been most frequently studied in that the prevalence of EDs was higher among females obese individuals are BED and BN (28). In our study, obese compared with males (13,14). Generally, females are people with dysglycaemia showed a higher prevalence very concerned about their weight, and it is somewhat of BED and BN than overweight, normal weight and common for adolescent girls to engage in inappropriate underweight participants; about 30% of the dysglycaemic weight management such as using laxatives, fasting participants who had BED were either overweight or and vomiting (35). Moreover, females are more likely to obese. report eating-related distress or loss of control because Several studies have identified factors that increase expressing emotions is sometimes more socially the risk of developing psychiatric problems that lead to accepted and expected from females (36). However, it is EDs (29,30). These include age, female sex, increased body also possible that males may not feel distressed or out of weight, body image dissatisfaction, history of dieting control when they overeat. and history of depression. In the current study, age and Physical activity is another risk factor for EDs. physical activity were associated with BN and BED in the Individuals with BED are commonly described as dysglycaemic group. Takii et al.. reported that individuals sedentary (37,38). In the current study, dysglycaemic with T1DM with an onset between age 7 and 18 years were patients who had a sedentary lifestyle had a higher at significantly higher risk of subsequently developing prevalence of BED and BN than patients with an active EDs such as AN or BN than those who were diagnosed lifestyle, which might be due to a number of factors, before 7 or after 18 years of age (31). The association of such as psychological and emotional factors, negative age with EDs in this study is in agreement with previous body attitude, social support, and the financial cost of the research (9,32); patients older than 18 years were 5 times exercise facility. Moreover, participants with a sedentary more likely to have BN than young patients who were less lifestyle are less likely to develop BED and BN than than 14 years old. In the nondysglycaemic group, age was people with an active lifestyle, which might be due to the only factor associated with other EDs such as atypical the fact that people with BED consider exercise a factor AN and purging disorders. Participants between 14–18 that allows them to eat greater quantities of food without years old were 2.6 times more likely to have other EDs. getting fat, while people with BN use exercise as a way Adolescence is a critical period of human development to overcome excessive food consumption. Individuals during which several physical and psychological changes with BED have been described as sedentary, whereas the occur, and peer influences and the continuous use of opposite has been the case for those with BN (38). social media may increase the risk of developing EDs in As a final point, the prevalence of EDs among this age group. diabetic patients showed incongruities. Many screening In the nondysglycaemic group, females were 4 times tools have been used to assess the existence of EDs; more likely to have BED compared with males. Studies however, they were used for different age groups and not conducted on BED have shown that girls had a higher designed for people who have medical conditions such as risk than boys (33,34). Research in Jordan has also shown diabetes. Thus, these tools might not display the actual

1506 Research article EMHJ – Vol. 26 No. 12 – 2020 estimate of EDs and might lead to a misclassification of abetes is difficult due to the frequent disguise and denial eating disorder risks in those with chronic illness. Another of disordered eating behaviour. Therefore, care providers limitation of this study is inherent in the cross-sectional must pay attention to warning signs such as poor gly- design: causality cannot be established using this design. caemic control and a refusal to be weighed. Screening is Further studies with the appropriate design are needed to recommended to secure early detection and subsequent establish the causal link between dysglycaemia and EDs. intervention. Conclusion Funding: This study was funded by the National Center for Diabetes, Endocrinology and Genetics, Amman, Jor- Adolescents with dysglycaemia showed a higher preva- lence of EDs compared with their nondysglycaemic peers dan. even though the diagnosis of EDs in individuals with di- Competing interests: None declared.

Étude comparative sur les troubles alimentaires chez les adolescents jordaniens avec et sans dysglycémie Résumé Contexte : Des études sur les troubles alimentaires chez les adolescents jordaniens ont fait état de taux de prévalence variables compris entre 12 et 40 %. Objectifs : La présente étude visait à déterminer la prévalence des troubles alimentaires chez les adolescents jordaniens avec et sans dysglycémie et à déterminer les facteurs qui y sont associés. Méthodes : Une étude transversale comparative a été menée au cours de la période allant de novembre 2017 à février 2018. L'échelle de diagnostic des troubles alimentaires a été utilisée pour évaluer la présence de différents types de troubles alimentaires, notamment l'anorexie mentale, la boulimie et l’hyperphagie boulimique. L'anorexie nerveuse atypique et le trouble de purge ont été considérés en tant « qu’autres troubles alimentaires » dans cette étude. Résultats : Cette étude portait sur 497 patients atteints de dysglycémie et 504 participants sans dysglycémie appariés selon l'âge. Les patients atteints de dysglycémie présentaient une prévalence significativement plus élevée de troubles de la boulimie par rapport aux participants sans dysglycémie (11,9 % contre 5,8 %, p < 0,001). Les adolescents atteints de dysglycémie âgés de 14 ans ou plus étaient plus susceptibles de souffrir de boulimie nerveuse que ceux de moins de 14 ans. Les patients ayant un mode de vie sédentaire étaient moins susceptibles de souffrir de boulimie et d’hyperphagie boulimique. Dans le groupe des sujets non dysglycémiques, la probabilité d'avoir d'autres troubles alimentaires était plus élevée ceux âgés de 14 à 18 ans. Les participants atteints de dysglycémie étaient plus susceptibles d'avoir une hyperphagie boulimique que ceux du groupe non dysglycémique (OR = 2,1, IC à 95 % : 1,3-3,3 ; p = 0,002) après ajustement en fonction des facteurs de confusion possibles. Conclusions : Les adolescents atteints de dysglycémie présentaient une prévalence plus élevée de troubles alimentaires par rapport à leurs pairs non atteints de dysglycémie. Le dépistage des troubles alimentaires est recommandé chez les adolescents afin d'assurer une détection précoce et une intervention ultérieure.

اضطرابات األكل بني املراهقني األردنيني املصابني بخلل سكر الدم وغري املصابني به: دراسة مقارنة هدى احلوراين، رنا أبابنة، هنلة خواجة، يوسف خرض، كامل العجلوين اخلالصة اخللفية: أفادت الدراسات التي ُأجريتعىل اضطرابات األكل بني املراهقني األردنيني أن معدالت االنتشار املتغرية ترتاوح بني 40%-12. األهداف: هدفتهذه الدراسة إىل حتديد معدل انتشار اضطرابات األكل بني املراهقني األردنيني املصابني بخلل سكر الدم وغري املصابني به، وحتديد العوامل املرتبطة بذلك. طرق البحث: ُأجريت دراسة مقطعية مقارنة خالل الفرتة من نوفمرب/ترشين الثاين 2017 إىل فرباير/شباط 2018. ُواست ِخدم مقياس تشخيص اضطرابات األكل لتقييم وجود أنواع خمتلفة من اضطرابات األكل، بام فيها فقدان الشهية العصبي، والنهام العصبي، واضطراب هنم الطعام. وأخذت الدراسة بعني االعتبار فقدان الشهية العصبي غري النمطي واالضطراب ُامل ِسهل "اضطرابات األكل األخرى". النتائج: شملت هذه الدراسة 497 ًمريضا يعانون من خلل سكر الدم و504 مشاركني من العمر نفسه ال يعانون من خلل سكر الدم. وكان معدلانتشار اضطراب هنم الطعام لدى املرىض املصابني بخلل سكر الدم أعىل بكثري ًمقارنة باملشاركني غري املصابني بخلل سكر الدم ≥ P )vs 5.8%, <0.001 (. ويف%11.9 جمموعة املصابني بخلل سكر الدم، كان املراهقون الذين بلغت أعامرهم 14 سنة أكثر ُعرضة لإلصابة بالنهام العصبي ًمقارنة بالذين تقل أعامرهم عن 14سنة. وكان املرىض الذين َّيتبعون نمط حياة يتسم بقلة احلركة أقل عرضة لإلصابة بالنهام العصبي

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واضطراب هنم الطعام. ويف جمموعة غري املصابني بخلل سكر الدم، كان أولئك الذين ترتاوح أعامرهم بني 14-18 سنة أكثر ُعرضة لإلصابة باضطرابات األكل األخرى. وكان أولئك الذين يعانون من خلل سكر الدم أكثر ُعرضة لإلصابة باضطراب هنم الطعام من أولئك الذين ينتمون إىل جمموعة غري املصابني بخلل سكر الدم (OR=2.1; 95% CI=1.3-3.3; p=0.002) بعد التصحيح من أجل السيطرة عىل عوامل اإلرباك املحتملة. كان االستنتاجات:معدل انتشار اضطرابات األكل لدى املراهقني املصابني بخلل سكر الدم أعىل ًمقارنة بأقراهنم الذين ال يعانون من خلل سكر الدم. َويوص بفحص املراهقني ِّللتحري عن اضطرابات األكل لضامن الكشف املبكر والتدخل الالحق.

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Does socioeconomic status influence oral cancer awareness? The role of public education

Somayyeh Azimi,1 Zahra Ghorbani,2 Erfan Ghasemi,3 Marc Tennant 1 and Estie Kruger 1

1International Research Collaborative, Oral Health and Equity, School of Human Sciences, University of Western Australia, Crawley, Australia. (Cor- respondence to: Somayyeh Azimi: [email protected]). 2Community Oral Health Department, Dental School; 3Department of Biostatistics, School of Paramedical Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Islamic Republic of Iran.

Abstract Background: Public awareness on oral cancer is thought to improve prevention and early diagnosis; however, the role of socioeconomic status in this awareness is not clear. Aims: The aim was to investigate whether an association exists between socioeconomic status and oral cancer awareness in adults. Methods: A multi-stage random sample of adults was investigated in Tehran in 2016–2017. The outcome was awareness of oral cancer and knowledge of risk factors and signs and symptoms using a self-administered questionnaire. The main exposures were self-reported socioeconomic status of 8 indicators of family assets and economic situation. Wealth index was created using principal component analysis, and participants were classified into 5 quintiles. Regression analysis was applied to test associations. Results: Out of 1800 adults, 1312 completed questionnaires were returned (72.8% response rate). The mean age was 37.8 (standard deviation 9.0) years; about 60% were female. Statistical analysis revealed the higher the wealth index, the higher the score for oral cancer knowledge and awareness. Awareness and knowledge were significantly lower among partici- pants in the poorest quintile: they had a knowledge score on oral cancer risk factors 1.58 points [95% confidence interval (CI): –2.19;–0.96] lower, and a knowledge score on oral cancer signs 1.34 points (95 CI: –1.98;–0.72) lower compared with the richest quintile. Conclusion: Socioeconomic inequalities were observed in oral cancer awareness in the Islamic Republic of Iran. Keywords: socioeconomic status; principal components analysis; oral cancer; awareness Citation: Azimi S; Ghorbani Z; Ghasemi E; Tennant M; Kruger E. Does socioeconomic status influence oral cancer awareness? The role of public educa- tion. East Mediterr Health J. 2020;26(12):1510–1517. https://doi.org/10.26719/emhj.20.060 Received: 04/09/18; accepted 29/12/20 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction public health researchers still debate of how SES is a factor in impaired health (1,5,12). The association between socioeconomic status (SES) and health outcomes has been widely documented in previ- In patients of lower SES, first presentation with ous studies (1–5). Evidence of inequalities in oral health more-advanced stages of oral cancer has been proposed has been repeatedly illustrated between and within as a possible association with disparity in oral cancer countries. Oral cancer, including cancer of the lip and burdens (13). Moreover, lack of or insufficient knowledge oral cavity, is not an exception, and recent global data has of oral cancer has been suggested as an effective factor shown differences in incidence and mortality in different in late diagnosis (13). Therefore, it could be proposed that countries (5–8). Global Cancer Incidence, Mortality and socioeconomic positon has an effect on awareness and Prevalence (GLOBOCAN) estimated 354 864 (2.0% of all knowledge about oral cancer, and in turn advanced stage sites) new cases of lip and oral cavity cancer, and 177 384 diagnosis. (1.9% of all sites) deaths worldwide in 2018. Age-standard- Previous studies have used various indicators, ized lip and oral cavity cancer incidence among men and single or combined, to measure SES, mostly focused women in Western Aisa has been reported to be 2.1 and 1.1 on occupation, education and income (14–17). However, per 100 000 (8). However, country-specific incidence and unavailable or unreliable results have been mentioned mortality rates have not been documented in this Region for income and occupation, especially in developing (7,9). countries (18). Ghorbani et al. developed an asset-based Associations between oral cancer risk and low SES SES index using principal component analysis (PCA) as (10), as well as the relationship between survival and a method for determining weights for the components mortality of oral cancer and both individual and area of a wealth index from a set of variables; they explored deprivation have been determined previously (11). Despite oral health inequalities in the Iranian population and some theoretical explanations for the disparity in health, suggested that household assets could be a good indicator

1510 Research article EMHJ – Vol. 26 No. 12 – 2020 for assessment of “long-run” economic status (18). plus some extra, money is not a problem) considering the There have been multiple studies assessing the levels previous studies (27,29,30). of awareness and knowledge of symptoms and risk Before finalizing the questionnaire, a pilot study was factors of oral cancer all over the world (19–21), however, conducted on a random sample of 60 patients attending most of them used sociodemographic measures such a dental school clinic to ensure clarity and practicability as age, sex and education as attributing factors. Also, a of the questions (α = 0.81). Eventually, the final Farsi review of the literature found that studies reporting oral language questionnaire we created fitted onto a double- cancer awareness in the Islamic Republic of Iran are rare sided plus one single A4 sheet stapled together. The with inconsistent results about sociodemographic factors purpose of the study and instructions were explained at (22–25). To the best of our knowledge, there is no study the beginning of the questionnaire. It took approximately associating wealth status and level of knowledge about 15 minutes to complete the questionnaire. oral cancer in a developing country. The aim of this study was to investigate the association between individual Sampling and participation wealth (by determining SES) and its association with In accordance with previous studies in the Islamic Re- awareness about oral cancer in the Islamic Republic of public of Iran in recent years (24), 16% was considered Iran. the proportion of knowledgeable patients (with regard to risk factors of oral cancer) for the sampling formula, and Methods we estimated that 1000 participants should be sufficient Background for the survey. Additional sampling was added in order to compensate for losses and refusals. This cross-sectional study is follow-up to an oral cancer knowledge study that was conducted in Tehran in 2016– The study population comprised adults who were 2017 using self-administered questionnaires (26). parents of public primary school students in Tehran. The sampling method used a multi-stage, stratified, Ethics random technique. First, from the 22 municipal regions The research project was approved by the ethics commit- in Tehran and according to geographic location, 4 regions tee of Shahid Beheshti University of Medical Sciences. were selected in the south, east, west, and north. Then, The purpose of the study was fully explained in the ques- were randomly selected 1 or 2 schools from the school tionnaire and responses to questions was on a voluntary list in each region. In each school, a grade was randomly basis. All participants were assured of anonymity and selected and the invitation letter sent to all the parents in confidentiality. that grade. The invitation letter was sent home with each student so both parents had the chance to see the letter. Questionnaire Study design The questionnaire assessed the awareness and knowl- edge of risk factors and symptoms of oral cancer as well A total of 1800 parents were invited to participate in this as socioeconomic status. It included demographic ques- study, which was conducted in Tehran in 2016–2017. tions (sex, age), 4 yes/no questions about oral cancer Those who agreed to participate were asked to sign the awareness (heard about cancer, non-communicable na- consent form. ture, early diagnosis and treatment); 15 questions about Participants were requested to return the completed knowledge of risk factors (tobacco, alcohol, sunlight, diet, the questionnaires on the same day, without any time genetics, age and human papilloma virus) and 11 ques- restrictions and to use their own knowledge, without tions about signs and symptoms (ulcers, red or white seeking information from online resources. Illiterate patches, swelling, difficulty swallowing, discomfort, persons, who were not able to write/read, were excluded change in voice and weight loss) (26). Oral cancer knowl- due to the self-administered nature of questionnaire. edge questions were closed-ended positive and negative A brochure containing information about oral and lip questions with yes/no/do not know options (27,28). The cancer was provided to all parents in the sampled schools questionnaire was designed by slightly modifying pre- after finishing the study. This brochure was approved vious valid questionnaires considering the local cultur- by the panel expert of community oral health and oral al, environmental and language environment (27,28). For medicine specialists in Shahid Beheshti University of assessment of SES, we used an 8-item composite wealth Medical Sciences, Tehran. index by adapting the existing validated asset questions (18), including house ownership (own/rent); yes/no ques- Outcome variables tions about having a car, personal computer, dishwasher, Awareness about oral cancer and knowledge of risk fac- steam-cleaner (a device to clean surfaces) and microwave; tors and signs and symptoms were collected using a nu- and questions about income satisfaction (How satisfied merical scale. Each correct answer was allocated a score are you with your current household income? Highly of 1; incorrect answers, including “do not know” answers satisfied, satisfied, dissatisfied, highly dissatisfied) and scored zero. The final scores for each participant were financial management (Do you have the ability to man- summed up separately: 0–4 for awareness, 0–15 for risk age expenditure with the available monthly income? can’t factor knowledge, and 0–11 for the signs and symptoms make ends meet, manage to get by, have enough money knowledge.

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Explanatory variables ticipants were female and 38% were male with the aver- age age 37.8 [standard deviation (SD) 9.0] years. The main explanatory variable was a composite wealth index as the proxy for SES; PCA was applied to indicator Mean score for awareness was 1.09 (SD 1.60) (out of variables and the samples classified into 5 equal wealth 4), for risk factors knowledge was 5.3 (SD 3.0) (out of 15), quintiles, where the first quintile represented the poorest and for signs and symptoms, knowledge was 4.5 (SD 2.9) 20% of the sample. (out of 11). Analysis indicated that oral cancer awareness and knowledge of oral cancer signs or risk factors were Covariates not significantly different between age categories. Male Age was recorded in date of birth and was categorised participants had less knowledge of oral cancer signs and into groups of 25–35, 35–45, and > 45 years. risk factors (P < 0.05), however awareness did not differ between males and females (Table 1). Statistics Principal component analysis revealed a single We used PCA to develop the wealth index using STATA, component with an Eigen-value > 1, covering 84% of version 11.1. Because the items included both binary and variance (data not shown). All variables included in this continuous variables, polychoric correlations were ap- factor had positive factor scores, and all were associated plied in the principal factor analysis correlation matrix. with higher socioeconomic status. Then the SES classification into 5 quintiles was conduct- Table 1 also demonstrates the relationship between ed via cluster analysis of the 8-item composite wealth SES and level of knowledge and awareness. There was using the data-driven approach. Descriptive and univari- ate analyses were used to explore the distribution of oral a statistically significant difference between level of cancer knowledge and awareness using SPSS, version awareness and knowledge of oral cancer risk factors 22. Statistical tests, including ANOVA and post hoc tests and signs and symptoms in the different socioeconomic and general linear regression were used for analysis of groups (P < 0.001). The post hoc test results showed the the level of knowledge and awareness among sociode- higher the wealth index, the higher the score for oral mographic groups. P < 0.05 was considered statistically cancer knowledge and awareness. significant in the survey. Table 2 shows general linear model analysis. The level of the wealth index remained statistically significantly Results associated with knowledge and awareness of oral cancer, Out of 1800 adults invited, 1312 completed questionnaires controlling for age and sex (Table 2). People from the were returned (72.8% response rate). In total, 62% of par- poorest quintile had a knowledge score on oral cancer

Table 1 Distribution of knowledge levels on oral cancer among 1312 adults in Tehran according to socioeconomic characteristics, 2016–2017 Characteristic Frequency General awareness Knowledge of risk Knowledge of factors signs No. (%) Mean (SD) Mean (SD) Mean (SD) Sex Male 489 (38.2 1.60 (1.09) 4.90 (2.92) 4.21 (2.96) Female 788 (61.7) 1.64 (1.01) 5.60 (3.00) 4.70 (2.88) P-valuea 0 562 < 0.001 < 0.001 Age (years) 25–35 318 (28.2) 1.60 (1.07) 5.26 (3.00) 4.38 (2.88) 35–45 644 (57.1) 1.68 (1.1) 5.44 (3.08) 4.68 (2.99) > 45 165 (14.6) 1.59 (1.0) 5.17 (2.83) 4.26 (2.88) P-valueb 0.4 0.50 0.16 Socioeconomic status quintilec 5th 204 (17.5) 1.92 (1.12) 6.23 (2.82) 5.09 (2.98) 4th 258 (22.2) 1.72 (1.03) 5.85 (2.87) 4.88 (2.92) 3th 207 (17.8) 1.72 (1.07) 5.45 (3.05) 4.60 (3.01) 2nd 262 (22.5) 1.54 (1.07) 4.95 (2.95) 4.35 (2.83) 1st 233 (20.0) 1.30 (1.02) 4.69 (2.97) 3.91 (2.68) P-valueb < 0.001 < 0.001 < 0.001

SD = standard deviation. aIndependent samples t-test. bAnalysis of variance test. c1st = poorest; 5th = richest.

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Table 2 General linear model regression results for oral cancer awareness among 1312 adults in Tehran according to socioeconomic status (SES), 2016–2017 Knowledge/ awareness SESa Bb P-value 95% confidence interval Lower bound Upper bound General awareness 1st –0.69 < 0.001 –0.91 –0.46 2nd –0.45 < 0.001 –0.67 –0.22 3th –0.27 0.02 –0.50 –0.04 4th –0.23 0.03 –0.45 –0.01 5th R Knowledge of risk factors 1st –1.58 < 0.001 –2.19 –0.96 2nd –1.43 < 0.001 –2.04 –0.82 3th –0.84 < 0.001 –1.48 –0.21 4th –0.39 0.20 –0.99 0.21 5th R Knowledge of signs 1st –1.34 < 0.001 –1.96 –0.72 2nd –0.83 < 0.001 –1.44 –0.22 3th –0.59 0.06 –1.22 0.03 4th –0.32 0.28 –0.93 0.27 5th R

All analyses adjusted for age and sex. R = reference. a1st = poorest; 5th = richest. bCoefficient estimate. risk factors 1.58 points [95% confidence interval (CI): because the SES and education level is higher in Tehran –2.19;–0.96] lower, and a knowledge score on oral cancer than other urban and rural areas across the country. signs 1.34 points (95% CI: –1.98;–0.72) lower compared Oral cancer, being a life-threatening disease, is with the richest quintile. usually diagnosed late. The survival rate may be Discussion improved significantly if the disease is diagnosed in the early stages or if the precancerous lesions are treated This study is one of the first epidemiological studies on (32). Our findings showed that the level of awareness of oral cancer awareness in the Islamic Republic of Iran, oral cancer risk factors was low. This is a crucial issue studying awareness of both risk factors and signs. Our in prevention of oral cancer as people do not even know findings indicate that oral cancer awareness is insuffi- which harmful behaviours and exposures may cause oral cient among the studied population, the mean scores cancer. Awareness is the first step, and it is the primary for both risk factors and signs being around 30% of the step towards changing attitudes and performance in this full scores. Mean general awareness score (1.09 out of 4) regard. We found that the level of awareness of oral cancer points to a lack of knowledge on oral cancer in adults. signs was low as well. This lack of information may lead Details have been provided in previous studies (26,31). to late diagnosis, hence affecting survival rates. The low Also, people in the lower SES quintiles had lower gener- level of public awareness of oral cancer has also been al awareness and less knowledge about risk factors and reported by other researchers from different countries, signs and symptoms of oral cancer. which reveals the need for education all around the world In light of the difficulties in accessing the adult (16,21,33). population to get a random sample, we tried to use public Another finding of this study was the lower awareness schools as the setting for sampling. Considering the among people from the low-SES group, who may have random selection of schools from different geographic limited access to knowledge sources about their health, areas of the huge city of Tehran, it seemed to achieve a large sample of adults in a low-cost way. Compared to the including information on oral cancer. This may be whole adult population, parents are of special importance; because of their lower level of educational attainment, an informed parent can affect the health of the whole lower level of health literacy and public education, and family, including the next generation. However, the less frequent physician/dental visits (34–36). parent population is not a representative sample of the A number of studies have evaluated the association adult population, making our findings ungeneralizable between sociodemographic indices such as age, sex, to the whole adult population of Tehran. The lack of education, occupation and level of knowledge of oral illiterate participants also affected generalizability. The cancer (33,37). Different studies reported inconsistent results may, however, be generalizable to Iranian parents results on the relationships between level of knowledge

1513 Research article EMHJ – Vol. 26 No. 12 – 2020 and sex and age. In the Islamic Republic of Iran, only In the current study, we used PCA for weighting Pakfetrat et al. reported significant differences in to construct a wealth index based on a previous study knowledge among people with different occupations (23). (5) and our results show the first component explained Occupation may not be a good indicator of SES due to the more than 80% of the original variables. The criteria for existence of income inequalities within an occupation, the selection of variables for PCA are not well defined, as well as high rates of women without formal jobs in and the number of selected components is arbitrary (42). developing countries. Tadbir et al., Pakfetrat et al., and In an Iranian study, Ghorbani et al., used PCA methods Gholami et al. reported the higher the education level, for measuring socioeconomic inequalities. They used the higher the score for oral cancer knowledge (22,23,25). the first component factor scores with coverage of 34% Although education is a good predictor of SES, it is not a of variance. Also, they classified the samples into 5 equal sole indicator of it. Income has been used as an indicator wealth quintiles, similar to this study (18). Krefis et al, in of SES in oral cancer knowledge studies before (17,33). a study in Ghana, used PCA asset-based wealth index for However, there are high non-response rates on items SES assessment with 20% coverage of the first component, directly measuring income, especially in developing and argued that combined SES indicators using PCAs countries due to cultural factors (18,38). provides a quantification and classification of individual In neighbouring countries, Al-Maweri et al. in SES levels and enables the use of the resulting score for Riyadh reported dental patients with lower SES were risk analyses (30). significantly less aware about oral cancer and had much Although a well-designed PCA analysis has been less knowledge of the signs and risk factors (39). Hassona set up as a suitable tool for assigning weights to et al. also reported people with lower SES in Jordan were the indicators in this study, all information on asset less well informed about the signs and risk factors of oral measures are based on self-reports of the participants, cancer (40). and were not confirmed by direct observation, and this In a recent study in the United Kingdom, Kawecki is considered a limitation. However, we asked questions et al., using the deprivation index, indicated lower about easily recalled ownership or appliances, which knowledge of mouth cancer in the most deprived areas reduces the possibility of recall bias. In addition, prices (41). These studies are in line with our study. However, are not taken into consideration in asset ownership, the measurement of SES can be different in different so, the appropriateness of the wealth index may differ populations. between regions. However, most previous studies used An asset-based approach, collecting information on this approach for construction of a wealth index (18,43). ownership of a range of durable assets, is an alternative Moreover, based on the multi-stage sampling design, it to traditional monetary indicators such as consumption is desired to run a multi-level regression model in any expenditure or income, for measuring SES (1,5). Ghorbani future analysis of the present data. et al. created an asset based wealth index for measuring Also, as a strength of this study, a brochure about oral health inequality in Tehran and demonstrated the oral cancer risk factors and sign and symptoms has low level of oral health in the poorest quintile (5). Also, been handed out in primary schools after the study, Islami et al. in the north of the Islamic Republic of Iran which can help parents as well as children acquire oral constructed an asset-based wealth index for assessing cancer-related knowledge, emphasizing the role of public SES and oesophageal cancer, and reported the protective education. effect of high wealth scores in the group with the highest A recent study in India used a mobile app for oral wealth status (top 20%) (38), which is in line with the cancer awareness in the general population. They argued current study. that mobile technology is used by all socioeconomic In the present study, a wealth index has been groups and the app can be used as a tool for patient developed using asset items, as well as 2 indirect education about prevention and early detection of oral monetary questions about financial management and cancer (44). income satisfaction. Previous studies have shown that people often refuse to discuss their income information Conclusion with others, and it is treated as sensitive or confidential, The results of this study demonstrate the advantage of however, income satisfaction questions dealt with the multiple variables rather than a single indicator of SES. emotional self-evaluation of income considering past The inverse association between combined indictors of or current income, or standard income relative to one’s SES and all components of oral cancer knowledge (gen- own merits and qualifications. Miething, in a survey in eral awareness, knowledge of risk factors and signs and Germany, argues that it could be an indicator of perceived symptoms) has been confirmed in the present study. inequality as well as a non-income-based exogenous Although improvement in SES is not achievable with- measure of income inequality (29). Also, financial out changing the general economy, dental public health management as the self-rated ability to manage with the policy makers should conduct active educational pro- available monthly income has been used as a component grammes, especially for the most deprived parts of the of measuring SES in previous studies (30). population to reduce the gap in oral cancer burden.

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Funding: This project was supported by the Dental ment research training programme scholarship from the School of Shahid Beheshti University of Medical Scienc- University of Western Australia. es in Tehran. Dr Azimi acknowledges the support of the Australian Government through an Australian Govern- Competing interests: None declared.

Influence du statut socio-économique sur le niveau de sensibilisation au cancer de la cavité buccale et rôle de l’éducation du public Résumé Contexte : La sensibilisation du public au cancer de la cavité buccale permettrait d’améliorer la prévention et le diagnostic précoce. On ignore cependant encore dans quelle mesure le statut socio-économique influence le niveau de sensibilisation. Objectifs : La présente étude visait à déterminer l’existence d’un lien entre le statut socio-économique et le niveau de sensibilisation au cancer de la cavité buccale chez les adultes. Méthodes : Un échantillon aléatoire à plusieurs degrés composé d’adultes a été analysé à Téhéran (République islamique d’Iran) en 2016-2017. Un questionnaire auto-administré a été distribué en vue d’évaluer le niveau de sensibilisation au cancer de la cavité buccale et la connaissance des facteurs de risque et des signes et symptômes. Pour évaluer le statut socio-économique, huit indicateurs portant sur le patrimoine familial et la situation économique ont été utilisés. Un indice de richesse a été créé en utilisant l’analyse en composantes principales et les participants ont été classés en cinq quintiles. Une analyse de régression a été appliquée aux associations de tests. Résultats : Sur les 1 800 adultes approchés, 1 312 ont rempli et retourné le questionnaire (taux de réponse de 72,8 %). L’âge moyen était de 37,8 ans (écart type 9,0) ; environ 60 % des participants étaient des femmes. L’analyse statistique a révélé que plus l’indice de richesse est élevé, meilleur est le niveau de connaissance et de sensibilisation à l’égard du cancer de la cavité buccale. Le niveau de connaissance et de sensibilisation était significativement plus faible chez les participants appartenant au quintile le plus pauvre : ils ont obtenu un score de connaissance sur les facteurs de risque du cancer de la cavité buccale inférieur de 1,58 point [intervalle de confiance à 95 % (IC) : –2,19 ; –0,96] et un score de connaissance sur les signes du cancer de la cavité buccale inférieur de 1,34 point (IC à 95 : –1,98 ; –0,72) par rapport au quintile le plus riche. Conclusion : Le statut socio-économique a une influence sur le niveau de sensibilisation au cancer de la cavité buccale en République islamique d’Iran.

هل تؤثر احلالة االجتامعية االقتصادية عىل الوعي برسطان الفم؟ دور التثقيف العام سمية عظيمي، زهرة قرباين، عرفان قاسمي، مارك تينانت، إستي كروجر اخلالصة اخللفية: ُي َدعتق أن الوعي العام برسطان الفم ِّيعزز الوقاية والتشخيص َاملبكر ْن، ومعي ذلك، فإن دور احلالة االجتامعية االقتصادية يف هذا الوعي غري واضح. األهداف: هدفت هذه الدراسة إىل ُّقمما التحقإذا كان هناك ارتباط بني احلالة االجتامعية االقتصادية والوعي برسطان الفم لدى البالغني. طرق البحث: ُاستقصيت ٌ عشوائيةعينة متعددة املراحل من البالغني يف طهران بجمهورية إيران اإلسالمية خالل الفرتة بني َعام ْي 2017-2016. ّومتثلت النتيجة يف الوقوف عىل مستوى الوعي برسطان الفم واملعرفة بعوامل اخلطر والعالمات واألعراض باستخدام استبيان ُي َستكمل ًذاتيا. ُ ُ َّوجتسدت حاالت ُّالتعرض الرئيسية يف احلالة االجتامعية االقتصادية ُامل َّبلغ عنها ً ذاتيالثامنية مؤرشات ِّملقومات األرسة والوضع االقتصادي. وأنشئ مؤرش الثروة باستخدام حتليل املكونات الرئيسية، ُوصنف املشاركون إىل 5 جمموعات. ُواستخدم حتليل االنحدار الختبار االرتباطات. النتائج: ِنم بني 1800 بالغ، تم تسليم 1312 ًاستبيانا َمستكم ًال )بمعدل استجابة %72.8(. وكان متوسط العمر 37.8 سنة )بانحراف معياري 9.0(، وبلغت نسبة اإلناث . %60وكشف التحليل اإلحصائي أنه كلام ارتفع مؤرش الثروة، ارتفعت درجة املعرفة والوعي برسطان الفم. وكانت درجة الوعي واملعرفة أقل بكثري لدى املشاركني يف الرشحية ُاخلمسية األكثر ًفقرا: كانت درجة معرفتهم بعوامل خطر اإلصابة برسطان الفم أقل بمقدار 1.58 نقطة ]فاصل الثقة (CI: = -2.19, -0.96 %95([، وكانت درجة املعرفة بعالمات رسطان الفم أقل بمقدار 1.34 نقطة 95% CI: = -1.98 -0.72) فاصل الثقة , ( ًمقارنة بالرشحية ُاخلمسية األكثر ًثراء. لوحظت االستنتاجات:أوجه تفاوت اجتامعية اقتصادية يف الوعي برسطان الفم يف مجهورية إيران اإلسالمية.

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26. Azimi S, Ghorbani Z, Tennant M, Kruger E, Safiaghdam H, Rafieian N. Population survey of knowledge about oral cancer and related factors in the capital of Iran. J Cancer Educ. 2017:1–8. doi:10.1007/s13187-017-1275-7 27. Posorski E, Boyd L, Giblin LJ, Welch L. Oral cancer awareness among community-dwelling senior citizens in Illinois. J Communi-� ty Health. 2014 Dec;39(6):1109–16. doi:10.1007/s10900-014-9862-6 28. Dodd VJ, Riley I, Joseph L, Logan HL. Developing an oropharyngeal cancer (OPC) knowledge and behaviors survey. Am J Health Behav. 2012;36(5):589–601. doi:10.5993/AJHB.36.5.2 29. Miething A. A matter of perception: exploring the role of income satisfaction in the income–mortality relationship in German survey data 1995–2010. Social Sci Med. 2013;99:72–9. 30. Krefis AC, Schwarz NG, Nkrumah B, Acquah S, Loag W, Sarpong N, et al. Principal component analysis of socioeconomic factors and their association with malaria in children from the Ashanti Region, Ghana. Malaria J. 2010;9(1):201. doi:10.1186/1475-2875-9- 201 31. Azimi S, Ghorbani Z, Ghasemi E, Tennant M, Kruger E. Disparities in oral cancer awareness: a population survey in Tehran, Iran. J Cancer Educ. 2019 Jun;34(3):535–41. doi: 10.1007/s13187-018-1337-5. 32. Sargeran K1, Murtomaa H, Safavi SM, Teronen O. Delayed diagnosis of oral cancer in Iran: challenge for prevention. Oral Health Prev Dent. 2009;7(1):69–76. PMID:19408818 33. Hertrampf K, Wenz H-J, Koller M, Wiltfang J. Public awareness about prevention and early detection of oral cancer: a popula- tion-based study in Northern Germany. J Cranio-Maxillofacial Surg. 2012;40(3):e82–e6. PMID:21592808 34. Mantwill S, Monestel-Umaña S, Schulz PJ. The relationship between health literacy and health disparities: a systematic review. PLoS One. 2015 Dec 23;10(12):e0145455. doi:10.1371/journal.pone.0145455 35. Matsuyama RK, Wilson-Genderson M, Kuhn L, Moghanaki D, Vachhani H, Paasche-Orlow M. Education level, not health literacy, associated with information needs for patients with cancer. Patient Educ Couns. 2011;85(3):e229–e36. doi:10.1016/j. pec.2011.03.022 36. Hovick SR, Liang M-C, Kahlor L. Predicting cancer risk knowledge and information seeking: The role of social and cognitive factors. Health Commun. 2014;29(7):656–68. doi:10.1080/10410236.2012.763204 37. Elango JK, Sundaram KR, Gangadharan P, Subhas P, Peter S, Pulayath C, et al. Factors affecting oral cancer awareness in a high- risk population in India. Asian Pac J Cancer Prev. 2009;10(4):627–30. PMID:19827883 38. Islami F, Kamangar F, Nasrollahzadeh D, Aghcheli K, Sotoudeh M, Abedi-Ardekani B, et al. Socio-economic status and oesoph- ageal cancer: results from a population-based case–control study in a high-risk area. International journal of epidemiology. 2009;38(4):978–88. doi:10.1093/ije/dyp195 39. Al-Maweri SA, Al-Soneidar WA, Dhaifullah E, Halboub ES, Tarakji B. Oral cancer: awareness and knowledge among dental pa- tients in Riyadh. J Cancer Educ. 2017 Jun;32(2):308–13. doi:10.1007/s13187-015-0924-y 40. Hassona Y, Scully C, Abu Ghosh M, Khoury Z, Jarrar S, Sawair F. Mouth cancer awareness and beliefs among dental patients. Int Dent J. 2015 Feb;65(1):15–21. doi:10.1111/idj.12140 41. Kawecki MM, Nedeva IR, Iloya J, Macfarlane TV. Mouth cancer awareness in general population: results from Grampian Region of Scotland, United Kingdom. J Oral Maxillofac Res. 2019 Jun 30;10(2):e3. doi:10.5037/jomr.2019.10203 42. Howe LD, Hargreaves JR, Huttly SR. Issues in the construction of wealth indices for the measurement of socio-economic posi- tion in low-income countries. Emerging themes in epidemiology. 2008;5(1):3. doi:10.1186/1742-7622-5-3 43. Homenauth E, Kajeguka D, Kulkarni MA. Principal component analysis of socioeconomic factors and their association with ma- laria and arbovirus risk in Tanzania: a sensitivity analysis. J Epidemiol Community Health. 2017 Nov;71(11):1046-1051. doi:10.1136/ jech-2017-209119 44. Deshpande S, Radke U, Karemore T, Mohril R, Rawlani S, Ingole P. A novel mobile app for oral cancer awareness amongst general population: development, implementation, and evaluation. J Contemp Dent Pract. 2019 Feb 1;20(2):190–196. PMID:31058634

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Tobacco price increase and consumption behaviour among male smokers in Saudi Arabia: a community-based study

Mohamad Al-Tannir,1 Amani Abu-Shaheen,2 Youssef Altannir 3 and Mustafa Altannir 3

1Research Monitoring Department, Research Center, Riyadh, Saudi Arabia. (Correspondence to: Mohamad Al- Tannir: [email protected]). 1King Fahad Medical City, King Fahad Medical City, Riyadh, Saudi Arabia. 2Scientific Writing Department, Research Center, King Fahad Medical City, Riyadh, Saudi Arabia. 3Research Monitoring Department, Research Center, College of Medicine, Alfaisal University, Riyadh, Saudi Arabia.

Abstract Background: Saudi Arabia doubled its tobacco tax in June 2017. Aims: To examine the association between an increase in tobacco prices and consumption behaviour among current male smokers in Riyadh. Methods: We conducted a community-based study using a self-administered questionnaire distributed to current male smokers aged 15+ years in Riyadh in 2018. The survey included questions on sociodemographic characteristics, tobacco consumption and self-reported chronic health conditions. Results: A total of 1481 participants were included in the final data analysis. After the tobacco tax was doubled, 25.6% of the participants reduced their cigarette consumption and 1.0% quit smoking. The average daily cigarette consumption af- ter enforcing the tobacco tax [19.77, standard deviation (SD) 10.7], was statistically significantly lower than before taxation (21.19, SD 10.8) (P < 0.0001). The calculated price elasticity of demand was −0.20 (inelastic). Employment status (P = 0.002) and per capita gross domestic product purchasing power parity (P = 0.001) were the only statistically significant factors associated with the change in smoking habits. Conclusions: Increasing tobacco prices reduced tobacco consumption by 26.6% among Saudi Arabian male smokers. Keywords: tobacco tax, tobacco consumption, male smokers, smoking habits, Saudi Arabia Citation: Abu-Shaheen A; Altannir Y; Altannir M. Tobacco price increase and consumption behaviour among male smokers in Saudi Arabia: a communi-� ty-based study. East Mediterr Health J. 2020;26(12):1518–1524. https://doi.org/10.26719/emhj.20.066 Received: 12/05/19, accepted: 30/12/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction increase their utilization because of a lack of social support, costs and access constraints (8). Also, clinicians Tobacco consumption is one of the biggest contributors were not likely to advise patients to quit or use smoking to public health problems, killing approximately 7 million cessation alternatives due to either time constraints with people worldwide each year (1). An average of 6 million deaths is attributable to the direct use of tobacco, while patients or inadequate training in delivering smoking an average of 890 000 deaths result from second-hand cessation services (8). smoking. According to global health observational data, Imposing taxes on tobacco products has proven to more than 1 billion people smoked tobacco in 2015, and be the most effective policy to reduce tobacco use and nearly 80% of them lived in low- and middle-income its adverse effects on health, the economy and society countries (1). (9–13). After joining the WHO Framework Convention for In 2016, the World Health Organization (WHO) in 2005, the Saudi Arabian Ministry of reported that the overall rate of tobacco use in Saudi Health initiated a national tobacco control programme Arabia among those aged 15+ years was 12.2%, with a rate with remarkable efforts. Saudi Arabia announced the of 23.7% among males compared with 1.5% among females doubling of tobacco tax on June 10, 2017 following the (2). In a previous survey of Saudi Arabian adolescents decision of the Gulf Cooperation Council countries. aged 13–15 years, the prevalence of tobacco use was 21.2% Increasing the price of tobacco products is considered among males and 9.1% among females (3). to be a highly effective policy to reduce tobacco use, Tremendous efforts have been made to reduce which eventually decreases the associated morbidity tobacco consumption all over the world in the form and mortality (14). Indeed, reducing tobacco use is a key of bans on smoking in public places, anti-smoking component of the Healthy People 2030 vision, part of the advertising campaigns, and comprehensive tobacco national action plan for improving the health of all Saudi control programmes (4–7). Arabians. The Gulf Cooperation Council governments provide This study aimed to assess the association between access to treatments such as nicotine the tobacco price increase due to higher tobacco taxes and replacement therapy (e.g. patch, inhaler, gum). However, consumption behaviour among current male smokers in the availability of these smoking alternatives did not Riyadh.

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Methods ulation across all districts of Riyadh and considering an incomplete and non-response rate of 20%, we would need Participants and questionnaire a sample of 1534 male smokers. The sample collected was A community-based cross-sectional study was conducted almost equal across the 5 districts: North 310, South 303, between April and October 2018 in all 5 districts of Riyadh East 308, West 308, Central 305. The sampling frame in- city (North, South, East, West, Central). Male smokers cluded coffee shops that had a seated smoking area. Site (current and those who quit after the tobacco tax in- visits and meetings with coffee shops managers were crease) aged 15+ years were eligible to participate. Males done in advance to acquire their approval for data col- below the age of 15 years, females, and males over 15 years lection. A convenience sample of 107 coffee shops was old who had never smoked were excluded. The study was reviewed for eligibility; 10 (9%) were determined ineligi- approved by the institutional review board at King Fahad ble due to the absence of an outdoor space designated for Medical City in Riyadh. smoking. An additional 5 (4.5%) coffee shops did not allow us to collect data on their premises. Therefore, data col- Participants were approached in coffee shops lection took place in 92 coffee shops: North 20, East 19, and other public places to take part in this study by South 18, West 18, Central 17. completing a self-administered questionnaire that was created based on an in-depth review of the literature (3,9– Statistical analysis 13). Considering the age categories, the sample size was Demographic characteristics of study participants were equally distributed across the 5 districts. The following reported as mean and standard deviation (SD) of a con- procedures were followed to ensure the validity of the tinuous variable, and categorical variables were reported questionnaire. First, the literature was reviewed and as number and percentage. previous instruments were examined to develop drafts of the questionnaire. The questionnaire was then reviewed Chi-squared was used to measure the association by 4 experts in research methodology and epidemiology. between the change in smoking habit (stopping, reducing, the average number of cigarettes per day) and Finally, to ensure the questionnaire was clear and well the covariates, including age, marital status, education, understood by the target population, a pilot study was employment status, and yearly income based on the GDP conducted on 50 Saudi Arabian males aged 15+ years per capita PPP in Saudi Arabia (US$ < 45821.61, ≥ 45821.61). recruited in coffee shops and other public places. Based For the multivariate analysis, a backward-elimination on the experts’ recommendations and the outcome of approach in a multiple logistic regression model was the pilot study, a few questions were reformulated and performed. Odds ratios and 95% confidence intervals amended to enhance the questionnaire’s validity. The were reported. The correlation coefficient, the standard pilot survey data were not included in the final analysis. deviation of the coefficient, andP -values were reported. The reliability, measured using Cronbach’s alpha, was We used SPSS, version 22, for data analysis and accounted 0.72. for the complex sampling design. A 2-tailed P-value of The questionnaire had 3 parts covering sociodemo- 0.05 was considered significant. graphic characteristics, tobacco consumption and self-re- The effect of increasing the tobacco tax on ported chronic health conditions. It took an average of 10 consumption behaviour was evaluated by calculating the minutes to complete. tobacco price elasticity. Sociodemographic characteristics included age group, The price elasticity of demand for tobacco was education level, marital status, employment status, and estimated using the ratio between the percent change in yearly income based on Saudi Arabia’s gross domestic the quantity demanded and the corresponding percent product (GDP) per capita purchasing power parity (PPP), change in price as in the formula below: equal to US$ 45 821 (14). Price elasticity of demand = percentage change in Tobacco consumption was assessed using 9 questions: quantity/percentage change in price opinion regarding the increase in tobacco prices, type of Percentage change in quantity = (Q − Q )/[(Q + Q )/2] tobacco consumed, change in consumption behaviour 2 1 2 1 × 100 based on the tax increase, change of cigarette brand to one with a cheaper price, number of cigarettes smoked Percentage change in price = (P2 − P1)/[(P2 + P1)/2] × 100 before and after taxation, number of years as a smoker, place where cigarettes are purchased, price of preferred Results type of tobacco, and current tobacco use. The final data set included 1481 out of 1534 male partici- pants since 53 questionnaires were excluded because of Sample size estimate extensive missing data. A total of 694 participants (47.0%) According to a 2016 census of the population of Riyadh, were in the 25–34 years age group, 821 (55.7%) were single, there were 3 747 557 males aged 15+ years. Given the prev- and 1168 (79.6%) were employed. Employment status (P = alence of smoking among this population is 25%, which 0.002) and GDP per capita PPP (P = 0.001) were the only equates to 936 889 smokers aged 15+ years. To generate statistically significant factors associated with a change a 95% confidence interval from a representative sample in smoking habits (Table 1). within a 2.5% margin of error, adjusting for the adult pop- The most common type of tobacco used was cigarettes

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Table 1 Association between participants’ demographic characteristics and changing in consumption behaviour, Riyadh, 2018 Characteristic Total Decreased smoking P-value No. % No. % Age (years) (n = 1477) 15–24 308 20.9 86 28.2 0.278 25–34 694 47.0 194 28.0 35–44 330 22.3 85 25.9 45–54 101 6.8 18 18.2 > 54 44 3.0 10 22.7 Education level (n = 1464) Elementary 7 0.5 1 14.3 0.463 Intermediate 23 1.6 7 30.4 Secondary 139 9.5 40 29.0 College 1090 74.4 280 25.8 Postgraduate 205 14.0 63 31.2 Marital status (n = 1475) Single 821 55.7 224 27.4 0.093 Married 599 40.6 160 26.9 Divorced 52 3.5 6 11.5 Widowed 3 0.2 1 33.3 Employment status (n = 1468) Employed 1168 79.6 295 25.4 0.02 Unemployed 300 20.4 95 32.0 GDP per capita PPP ($US) (n = 1387) < 45 821.61 1009 72.9 288 28.7 0.001 ≥ 45 821.61 375 27.1 77 20.6

GDP = gross domestic product; PPP = purchasing power parity. P < 0.05 considered significant in 1269 (85.7%). We found that 372 participants (25.1%) participants with a GDP per capita PPP below 45 821.61 agreed with the increased taxes on cigarettes versus USD were 1.45 times more likely to stop or significantly 896 participants (60.5%) who disagreed. After taxes were reduce the average number of cigarettes smoked per day increased, 379 participants (25.6%) reduced cigarette compared with participants with a higher GDP per capita consumption and 15 (1.0%) quit smoking. The daily mean PPP (P = 0.01). Employment status was also a significant cigarette consumption before the tax increase was 22.19 factor that affected tobacco consumption behaviour (SD 10.8) compared with 19.77 (SD 10.70) afterwards (P among the study participants. The employed participants < 0.0001). The mean price of cigarettes before and after were less likely to stop or reduce smoking in comparison the tax increase was US$ 3.68 (SD 4.59) and US$ 6.63 (SD with unemployed participants (odds ratio: 0.72, P = 0.04) 4.96) respectively. Respondents’ smoking characteristics (Table 3). are presented in Table 2: 375 (25.3%) purchased cigarettes from both local markets and duty-free shops, and 110 Discussion (7.4%) from duty-free shops only. A decrease in cigarette consumption could result from The calculated tobacco price elasticity was (−0.20): reducing the number of cigarettes consumed per smok- Change in quantity = (22.9 – 19.77)/(22.19 + 19.77)/2 × er or by reducing the number of smokers. The results of 100 = 14.9% our study showed that increasing the prices of tobacco products was associated with a significant reduction in Change in price = (6.63 – 3.68)/(6.63 + 3.68)/2 × 100 = the number of cigarettes consumed by smokers. 57.2% According to our findings, a 100% increase in tobacco Price elasticity of demand = 11.53/57.22 = 0.20 tax reduced tobacco consumption by 26.6% among The demand for tobacco is, therefore, said to be price our participants. This is consistent with previous inelastic; this means that tobacco consumption behaviour studies documenting that increasing cigarette prices is unresponsive to a change in price. through taxation is one of the most effective methods From the multivariate analysis, we determined that of decreasing cigarette consumption (15–20). Several

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Table 2 Characteristics of participant smokers, Riyadh, 2018 Characteristic No.a %a Increase tobacco price (n = 1474) Agree 370 25.1 Disagree 892 60.5 No comment 212 14.4 Type of tobacco (n = 1481) Cigarettes 1269 85.7 Hookah (water pipe) 128 8.6 Electronic cigarettes 52 3.5 Cigar 16 1.2 Pipe 5 0.3 Other 11 0.7 Change in consumption behaviour (n = 1481) Stopped 15 1.0 Reduced 379 25.6 Change to a cheaper brand 223 15.1 No change 1087 73.4 Mean (SD) no. of cigarettes before taxation increase 22.19 10.8 Mean (SD) no. of cigarettes after taxation increase 19.77 10.7 Mean (SD) no. years of smoking 12.22 8.5 Source of cigarettes (n = 1481) Local market 979 66.1 Duty free 110 7.4 Both 375 25.3 Other 17 1.2 Mean price of cigarettes pack before taxation ($US) 3.68 ±4.59 Mean price of cigarettes pack after taxation ($US) 6.63 ±4.96 aExcept where indicated as mean and standard deviation (SD). countries have started to implement such taxes after these an increase in cigarette prices on consumption. The study positive results were observed (19–31). Numerous studies showed that the price elasticity of cigarette demand varied in high-income countries have shown that a 10% increase from −0.503 to −1.227 in those countries. Countries with in cigarette prices decreases consumption by about 4% a per capita gross national income below US$ 5418 had (32). Available data indicate that consumption in low- the highest cigarette price elasticity (−1.227). Those with and middle-income countries is even more responsive to a per capita gross national income greater than US$ 5418 price. For example, estimated decreases were about 5.5% exhibited less cigarette price elasticity (20). In our results, in China, 5.2% in Mexico, and 5.4% in South Africa (17–19). GDP per capita PPP and employment status were In economics, price elasticity is defined as the shown to significantly affect smoking habits among the percentage change in consumption in response to a participants. Employed participants with a higher GDP 1% change in price. The price elasticity of demand is a per capita PPP were less likely to stop smoking or reduce measure to show the responsiveness, or elasticity, of their consumption of tobacco after the tax increase. The the quantity of a good or service, demanded by a given 2 primary concerns that have been expressed relative to change in its price. In our study, the demand for smoking this tax increase were: an increase in smuggling to avoid is classed as inelastic (–0.20). Inelastic demand indicates the additional tax burden; the most common strategy low responsiveness to price changes, which suggests for tax avoidance was purchasing cigarettes from duty- that after the tax increase, cigarettes are still affordable. free shops; our data showed that 25.3% of respondents Future increases in cigarette prices might increase the purchased cigarettes from both local markets and duty- price elasticity, which could suggest a more effective use free shops and 7.4% from duty-free shops only; and of tax increases to control tobacco. A study employing secondly, smokers switching to cheaper alternatives and panel data for the period 2005–2014 from Euromonitor lower quality tobacco products, which was expressed by International, the World Bank and WHO in the 28 15% of our study participants. countries of the European Union explored the effects of The majority of our respondents disagreed about the

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Table 3 Multivariate analysis of the statistically significant variables Characteristic Coefficient SD of the P-value Odds ratio 95% CI coefficient

Employed –0.06 0.403 0.02 0.72 0.53–0.98 GDP per capita PPP $US < 45 821.61 0.08 0.443 0.003 1.45 1.08–1.95

SD = standard deviation; CI = confidence interval. GDP = gross domestic product; PPP = purchasing power parity. P < 0.05 is considered significant. increase in the price of tobacco products. Similarly, a study as the use of addictive substances, including smoking conducted by Green and Gerken showed that smokers cigarettes, is considered deviant behaviour among female disagreed more often with increases in tobacco taxation Saudi Arabians. Thus, the results of this study cannot compared to nonsmokers (29). Another study conducted be generalized to the entire Saudi Arabian population. by Dixon et al. reported that the relationship between Finally, the reliability of the data is dependent on the income difference and support for higher tobacco respondents’ recall and honesty. Underreporting of the sales taxes was considered minor for nonsmokers, but number of cigarettes smoked before and after the tax essential for smokers (30). increase could also be a significant problem. Public health authorities need to promote educational programmes to provide youth with knowledge about Conclusion tobacco hazards, and to further assist and provide needed Although increasing tobacco prices reduced tobacco con- guidance and support to tobacco consumers who are willing to quit. Many policy-makers in other countries sumption by 26.6% among Saudi Arabian male smokers, use some of the revenue produced from tobacco taxes cigarette price elasticity was less than 1. The results of the to support anti-smoking activities. For instance, the study might be important for policymakers to develop a California Tobacco Tax and Health Promotion used strategic plan to adopt new measures to control smoking. tobacco tax revenue to develop educational programmes Furthermore, there is a need to design and develop ed- to prevent and reduce cigarette use (22). In Australia, a ucational programmes to enhance the knowledge of the 5% tax on the sale of tobacco products is used to support community regarding the negative impact of smoking on health promotion programmes (21). In Egypt and Nepal, health. Future research is needed in this area, especially additional tax revenues were used in health-related in the Middle East and specifically in Saudi Arabia, be- activities to support health care for children and low- cause published studies in this field are relatively scarce. income families (21). Funding: This study was funded by the research centre Our study is subject to certain limitations. First, at King Fahad Medical City. smoking variables were self-reported without biomarker validation. Second, this study was done only on males Competing interests: None declared.

Hausse du prix du tabac et comportements de consommation chez les fumeurs masculins en Arabie saoudite : enquête en communauté Résumé Contexte : L’Arabie saoudite a doublé sa taxe sur le tabac en juin 2017. Objectifs : Examiner le lien entre la hausse du prix du tabac et les comportements de consommation des fumeurs masculins à Riyad. Méthodes : En 2018, nous avons mené une enquête en communauté à Riyad en distribuant un questionnaire auto- administré à des fumeurs masculins âgés de 15 ans et plus. L’enquête comprenait des questions sur les caractéristiques sociodémographiques, la consommation de tabac et les maladies chroniques autodéclarées. Résultats : Au total, 1 481 participants ont été pris en compte dans l’analyse finale des données. Après le doublement de la taxe sur le tabac, 25,6 % des participants ont réduit leur consommation de cigarettes et 1,0 % ont cessé de fumer. La consommation quotidienne moyenne de cigarettes après l’imposition de la taxe sur le tabac (19,77 ; écart type : 10,7) était, d’un point de vue statistique, significativement plus faible qu’avant son imposition (21,19 ; écart type : 10,8) (p < 0,0001). L’élasticité-prix de la demande était de −0,20 (inélastique). Le statut professionnel (p = 0,002) et le produit intérieur brut par habitant mesuré en parité de pouvoir d’achat (p = 0,001) ont été les seuls facteurs statistiquement significatifs associés au changement des habitudes tabagiques. Conclusions : La hausse des prix a réduit de 26,6 % la consommation de tabac des fumeurs masculins saoudiens.

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ارتفاع أسعار التبغ والسلوك االستهالكي يف صفوف املدخنني الذكور يف الرياض: دراسة جمتمعية حممد التنري، أماين أبو شاهني، يوسف التنري، مصطفى التنري اخلالصة اخللفية: ضاعفت اململكة العربية السعودية الرضيبة التي تفرضها عىل التبغ يف يونيو/حزيران 2017. األهداف:هدفتهذه الدراسة إىل دراسة العالقة بني زيادة أسعار التبغ والسلوك االستهالكي يف صفوف املدخنني الذكور احلاليني يف الرياض. طرق البحث: أجرينا دراسة جمتمعية باستخدام استبيان ُي َستكمل ًذاتيا ُو ِّععىل زاملدخنني الذكور احلاليني الذين تبلغ أعامرهم 15 سنة فام فوق يف الرياض يف عام 2018. َّوتضمن املسح ًأسئلةحول اخلصائص االجتامعية السكانية، واستهالك التبغ واحلاالت الصحية املزمنة ُامل َبلغ عنها ًذاتيا. النتائج: َّضم التحليل النهائي للبيانات ما جمموعه 1481 ً.مشاركا وبعد مضاعفة رضيبة التبغ، َّخفض من%25.6 املشاركني استهالكهم للسجائر، وأقلع %1.0 منهم عن التدخني. وكان متوسط االستهالك اليومي للسجائر بعد إنفاذ رضيبة التبغ ]19.77، االنحراف املعياري 10.7[ أقل بكثري من االستهالك قبل إنفاذ الرضيبة من الناحية اإلحصائية )21.19، االنحراف املعياري ( 10.8)القيمة االحتاملية > 0.0001(. وكانت مرونة السعر املحسوبة للطلب 0.20- )غري مرن(. وكانت حالة التوظيف )القيمة االحتاملية = ( 0.002وتعادل القوة الرشائية للفرد يف الناتج املحيل اإلمجايل )القيمة االحتاملية = 0.001( العوامل الوحيدة ذات الداللة اإلحصائية املرتبطة بالتغ ُّري يف عادات التدخني. االستنتاجات: َّأدت زيادة أسعار التبغ إىل خفض استهالك التبغ بنسبة %26.6يف صفوف املدخنني الذكور يف اململكة العربية السعودية.

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16. Hu T-w, Mao Z, Shi J, Chen W. Tobacco taxation and its potential impact in China. Paris: International Union Against Tuberculo- sis and Lung Disease; 2008. 17. Waters H, Sáenz de Miera B, Ross H, Reynales Shigematsu LM. The economics of tobacco and tobacco taxation in Mexico. Paris. International Union Against Tuberculosis and Lung Disease; 2010. 18. Van Walbeek C. Tobacco excise taxation in South Africa. Johannesburg: World Health Organization; 2003. 19. Yeh CY, Schafferer C, Lee JM, Ho LM, Hsieh CJ. The effects of a rise in cigarette price on cigarette consumption, tobacco taxation revenues, and of smoking-related deaths in 28 EU countries-- applying threshold regression modelling. BMC Public Health. 2017 Sep 21;17(1):676. doi:10.1186/s12889-017-4685-x 20. Hu TW: Cigarette taxation in China: Lessons from international experiences. Tob Control. 1997;6:136–40. 21. Bal DG, Kizer KW, Felten PG, Mozar HN, Niemeyer D. Reducing tobacco consumption in California. Development of a statewide anti-tobacco use campaign. JAMA. 1990 Sep 26;264(12):1570–4. PMID:2395199 22. Goldstein AO, Cohen JE, Flynn BS, Gottlieb NH, Solomon LJ, Dana GS, et al: State legislators’ attitudes and voting intentions toward tobacco control legislation. Am J Public Health. 1997;87:1197–200. doi:10.2105/ajph.87.7.1197 23. Hahn EJ, Toumey CP, Rayens MK, McCoy CA: Kentucky legislators’ views on tobacco policy. Am J Prev Med. 1999;16:81–8. doi:10.1016/s0749-3797(98)00134-2 24. Hahn EJ, Rayens MK: Consensus for tobacco policy among former state legislators using the policy Delphi method. Tob Control. 1999 Summer;8(2):137–40. doi:10.1136/tc.8.2.137 25. Keeler TE, Hu TW, Barnett PG, Manning WG: Taxation, regulation, and addiction: a demand function for cigarettes based on time-series evidence. J Health Econ. 1993 Apr;12(1):1–18. doi:10.1016/0167-6296(93)90037-f 26. Lanoie P, Leclair P. Taxation or regulation: looking for a good anti-smoking policy. Economics Letters. 1998;58:85–9. https://doi. org/10.1016/S0165-1765(97)00258-9 27. Jeffery RW, Forster JL, Schmind TL, McBride CM, Rooney BL, Pirie PL. Community attitudes toward public policies to control alcohol, tobacco, and high fat food consumption. Am J Prev Med. 1990 Jan–Feb;6(1):12–9. PMID:2340187 28. Pederson LL, Shelley BB, Ashley JJ. A population suvery on legistlative measure sto restric smoking in Ontario: 2. Knowledge, attitudes and predicted behavior. Am J Prev Med. 1986 Nov–Dec;2(6):316–23. PMID:3453196 29. Green DP, Gerken AE: Self-interest and public opinion toward smoking restrictions and cigarette taxes. Public Opinion Quarterly. 1989;53:1–16. https://doi.org/10.1086/269138 30. Dixon RD, Lowery RC, Levy DE, Ferraro KF. Self-interest and public opinion toward smoking policies: a replication and exten- sion. Public Opinion Quarterly. 1991;55:241–54. https://doi.org/10.1086/269255 31. WHO technical manual on tobacco tax administration. Geneva: World Health Organization; 2010.

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Relative risk of injury due to alcohol consumption in car and motorcycle drivers

Mahnaz Yadollahi 1 and Forough Pazhuheian 1

1Trauma Research Center, Shahid Rajaee Hospital, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. (Correspondence to: M. Yadollahi: [email protected]).

Abstract Background: There is strong evidence that a substantial number of fatal as well as nonfatal injuries in road traffic acci- dents result from alcohol consumption and abuse. Aims: To examine the relationship between blood alcohol concentration and characteristics of injury in trauma patients admitted to a major teaching hospital. Methods: This was a cross-sectional investigation of trauma characteristics among 38 435 car and motorcycle drivers referred to the South of Iran Trauma Center between October and March 2018. A log-binomial regression model was used to evaluate the relative risk of each covariate on the Injury Severity Score. Results: There were 253 patients (7.78%) with alcohol consumption. Also, blood alcohol level was positive in 8.66% and 6.93% of car and motorcycle drivers, respectively. The ISS in alcohol consumers and nonconsumers was 6.34 (standard de- viation; 8.73) and 4.12 (7.78), respectively, which was significantly higher in the alcohol consumers t( test = 12.96, P < 0.001). Therefore, alcohol consumption was a significant factor in increasing the relative risk of injury, which was 2.83 units more than among drivers who had not consumed alcohol. Conclusions: Our findings show that the police and law enforcement agencies have a responsibility to enforce stricter rules to reduce drink driving and the burden of trauma on the healthcare system. Keywords: drink driving, traffic accident, Injury Severity Score, Islamic Republic of Iran Citation: Yadollahi M; Pazhuheian F. Relative risk of injury due to alcohol consumption in car and motorcycle drivers. East Mediterr Health J. 2020;26(12):1525–1531. https://doi.org/10.26719/emhj.20.057 Received: 04/06/19; accepted: 22/09/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction No specific study has determined the prevalence of alcohol-related injuries in RTAs in the Islamic Republic Road traffic accidents (RTAs) are the leading cause of of Iran where, as a Muslim-majority country, alcohol is death and disability among people aged 20–50 years (1). illegal. Moreover, no study has reported the consequences Despite improved hospital care, mortality from RTAs is of alcohol consumption and other demographic variables the second leading public health problem in the Islamic on severity of injury in RTAs. The aims of this study were Republic of Iran (2). There is strong evidence that a sub- to determine the prevalence of alcohol consumption stantial number of fatal as well as nonfatal injuries re- in car and motorcycle drivers involved in RTAs and sults from alcohol consumption and abuse (3); therefore, to compare the severity of injuries between alcohol it can be argued that alcohol consumption is one of the consumers and non-consumers. We also compared the most well-known risk factors for RTAs (4,5). High alco- prevalence of drink driving in the Islamic Republic of hol consumption was attributed to 14% of all road traffic Iran to that in other Muslim-majority countries in the injuries and the rate of alcohol consumption in RTAs has Middle East and countries in which alcohol is legal. been reported to vary from 14% to 26% (4,6). It is reported that the chance of an accident after alcohol consumption Methods is 6.1 times higher than without alcohol consumption (7). Among the Iranian population in 2015, the prevalence rate This was a retrospective cohort investigation of trauma of substance use was 2.65% in people aged 15–64 years characteristics among car and motorcycle drivers in- and the approximate number of addicts was estimated­ to volved in RTAs who were referred to Shahid Rajaee Trau- be 1 325 000 (8). Despite strict rules and prohibitions on ma Center (Emtiaz) between October and March 2018. We consuming, buying and selling of alcohol in the Islamic excluded patients aged < 15 years; patients who were dis- Republic of Iran, the prevalence of alcohol consumption charged or died within 24 hours; patients dead on arrival among young educated people is still increasing (9). Al- at hospital; patients without the data necessary to calcu- though studies have found a direct correlation between late their trauma score; patients whose Abbreviated Inju- alcohol and mortality (10,11), the effect of blood alcohol ry Scale (AIS) values were not measurable; patients with level on Injury Severity Score (ISS) has not been meas- unclear type of trauma; and patients with mild injuries ured when this group is matched with drivers who do such as soft tissue damage and fractures. not consume alcohol (12). Alcohol consumption was determined by measuring

1525 Research article EMHJ – Vol. 26 No. 12 – 2020 blood alcohol level in a diagnostic laboratory. ISS was Although this is often appropriate, there may be considered as the outcome variable. ISS was based on situations in which it is more desirable to estimate a radiological findings and the International Statistical relative risk or risk ratio (RR) instead of OR. With minor Classification of Diseases, 10th revision (ICD-10) codes. modification of the statements for logistic regression, a Demographic data including age, sex, type of driver, log-binomial model can be run to obtain the RR instead of time of admission to hospital, duration of hospitalization, the OR. All that needs to be changed is the link function and ISS were studied. Experts calculated severity between the covariates and outcome (13). Therefore, a log- by referring to patients’ medical records, including binomial regression model was used to evaluate the RR of diagnostic ICD-10 codes, surgical reports, primary triage each covariate in ISS (divided into ISS ≤ 8 vs ISS > 8 based papers and emergency reports. Each ICD-10 injury code on distribution of injury severity). A 2-sided P < 0.05 was was assigned to one of the 6 ISS body regions. According to considered statistically significant. Data were analysed the AIS, each patient’s injured body regions corresponded using Stata14 software and figures were prepared using to the injured body region with the highest ISS. In this R 3.4.3 for Windows. regard, all injuries received an AIS code ranging from 1 This project was approved by the Research Ethics (minor injury) to 6 (an injury considered incompatible Committee with number of IR.SUMS.REC.1397.420 by with life). Patients with multiple injuries were scored by Shiraz University of Medical Sciences in Shiraz, Islamic adding the squares of the three highest AIS scores in 3 Republic of Iran. predetermined body regions. This process provided the ISS which ranged from 1 to 75. Additionally, because there Results was no information on alcohol consumption in patients’ There were a total of 38 435 injured patients, which in- records, this information was based on the patients’ cluded 253 (7.78%) who were positive for alcohol con- admission code. sumption. Blood alcohol level was positive in 8.66% of Statistical methods such as chi2 test, two independent car and 6.93% of motorcycle drivers involved in RTAs. t tests, and one-way analysis of variance were used for The average age of alcohol users was 26.16 (7.98) descriptive comparisons of demographic characteristics years, 95.26% of whom were male and 4.7% female and clinical indicators in alcohol and non-alcohol (Table 1). The ISS in alcohol users was 6.34 (8.73) and consumers. Binary outcomes in cohort studies are there was a significant difference between the alcohol commonly analysed by applying a logistic regression consumers and nonconsumers. The number of people model to the data to obtain odds ratios (ORs) for with ISS > 8 was greater among alcohol consumers than comparing groups with different sets of characteristics. nonconsumers (26.49% vs 15.01%). The highest number of

Table 1 Comparison of demographic and clinical features (stratified by alcohol consumption) Variables Alcohol consumption No alcohol consumption P (253) (2998) Age, mean (SD) 26.16 (7.98) years 33.02 (13.85) years < 0.001 Sex 0.045 Male 241 (95.26) 2749 (91.69) Female 12 (4.74) 249 (8.31) Type of driver 0.066 Car 139 (54.96) 1467 (48.93) Motorcycle 114 (45.06) 1531 (51.07) Injury severity score, mean (SD) 6.34 (8.73) 4.12 (7.78) < 0.001 1–4 156 (61.66) 2371 (79.09) 5–8 30 (11.86) 177 (5.9) 9–15 39 (15.42) 247 (8.24) 16–25 17 (6.72) 146 (4.87) > 25 11 (4.35) 57 (1.90) Time of accident < 0.001 20:00–04:00 204 (80.63) 1093 (36.46) 04:00–12:00 19 (7.51) 560 (18.68) 12:00–20:00 30 (11.86) 1345 (44.86) Injured patients per day, mean (SD) < 0.001 In holidays 2.04 (0.34) 16.31 (0.56) In non-holidays 0.79 (0.07) 11.55 (0.12)

SD = standard deviation

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Table 2 Relative risk of injury based on covariates Variables RR Z statistic P 95% CI for RR Lower Upper Age 1.01 2.91 0.04 1.00 1.01 Sex (Female to Male) 2.16 4.27 < 0.001 1.51 2.09 Type of driver (motorcycle driver to car drivers) 0.6 -6.69 < 0.001 0.65 0.72 Alcohol 2.83 -44.06 < 0.001 1.54 2.17

CI = confidence interval; RR = relative risk. accidents (80.63%) among alcohol consumers occurred positive result for alcohol consumption at the time of the between 20:00 and 04:00 hours. The average number of accident. As age increased, the number of accidents also patients injured daily was significantly greater during decreased among alcohol users. holidays in comparison to working days for both alcohol consumers and nonconsumers. Discussion A log-binomial regression model was performed to The current study evaluated the effect of alcohol con- determine the relative risk of covariates on ISS (Table sumption on severity of injury in drivers involved in 2). The predictive variables were age, sex, type of driver RTAs. The relationship between percentage of alcohol (motorcycle or car) and alcohol consumption and the consumption and increased risk of accident was evaluat- independent variable was ISS. Increasing age with control ed using log-binomial regression. of other variables led to a 0.01 increase in risk of ISS in The prevalence of alcohol consumption while driving > 8 patients. The risk of severe injury was significantly was 7.78% in our study, which is less than in other studies. higher in motorcycle compared to car drivers. Alcohol The results of a study in US National Trauma Data consumption was a significant factor in increasing the Bank (2007–2010) indicated that among a total of 88 794 relative risk which was 2.83 units more in comparison to motorcycle drivers, 30.9% showed positive test results for that in non-alcohol consumers. alcohol (14). A study in Virginia, United States of America showed that prevalence of alcohol consumption while A closer look at the alcohol titer among surviving driving was about 36.89% (15). In Australia, blood alcohol patients indicates that the severity of injury increased was present in 29.1% of all drivers (16). In a study of RTAs with alcohol consumption and it was higher in motorcycle in Turkey, alcohol was detected in the blood of about than car drivers (Figure 1). 54.4% of cases, although subjects were considered to be Figure 2 shows the percentage of accidents among positive when alcohol blood concentration exceeded drinkers in each age group. The percentage of accidents 50 mg/dl (17). In other studies the prevalence of alcohol in alcohol users was higher among younger drivers. in drivers was lower than in our study. A study in the About 12% of injured drivers aged 15–20 years had a United Arab Emirates found that the prevalence of

Figure 1 ISS stratified by blood alcohol level

10.0

7.9 Motorcycle accident 7.5 6.54 6.55 Car accident 5.65 5.0 4.11

2.81 2.5 Mean of injury severity score injury of severity Mean

0.0

Negative alcohol 80- 150 More than 150 Blood alcohol level (mg/dl) ISS = Injury Severity Score

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Figure 2 Percentage of accidents among drinkers by age groups

12.5

10.0

7.5

5.0

Percentage of accidents of Percentage 2.5

0.0 15-20 21-25 26-30 31-35 36-40 41-45 46-50 More than 50 Age group alcohol consumption in car drivers was about 2.2% (18). is consistent with a study of alcohol consumption in Also, prevalence of alcohol among injured drivers was Denmark (25). reported as 0.45% in Norway (19). In a study in Qatar, A log-binomial regression model was used in this study the prevalence of driving while under the influence of to analyse injury severity due to alcohol consumption in alcohol was estimated as 1.8% (20). A study in Singapore RTAs, with control of other variables. Hoong et al. have showed that 2.3–3.0% of fatal and injury-sustaining used this model to evaluate occurrence of RTAs at road RTAs were alcohol related (21). The differences in alcohol intersections for several years and have shown that consumption patterns in different countries are due to the log-binomial model is more effective than survival stringent laws as well as religion. Moreover, it should be models for evaluation of relative risk of injury (26). Our noted that our study considered blood alcohol > 80 mg/ study can pave the way for developing theories about the dl as alcohol consumption. The permissible amount of reasons behind the high incidence of RTAs due to alcohol alcohol in the blood differs between countries; in some it consumption in holidays. As a result of higher injury is 100 mg/dl and in others it is 50 mg/dl. severity among alcohol consumers, we recommend that Our results revealed that consumption of alcohol greater supervision is needed regarding high-risk driving increased ISS by 2.8 times to > 8 compared to behaviour. We also advise law enforcers to implement nonconsumers. Our results are consistent with those stricter laws concerning the ban on alcohol consumption. of Valdez et al., who showed that blood alcohol level is The limitations of our study include the fact that associated with ISS for specific types of injuries; however, we were not able to determine the type of body injuries across all types of injuries, there was no significant compared to injury severity in different parts of the association between blood alcohol level and ISS (22). body. Moreover, data about deaths at the scene as well We found that ISS in motorcycle drivers was higher as prehosital deaths, type of car, speed, seat belt use and than that in car drivers. This is consistent with the studies drowsy driving were not available. The effect of these of Bolandparvaz et al., who reported injury patterns varibles as well as opioid substances should be evaluated among trauma patients of different ages and sex in the in future studies for evaluation of competitive risks Islamic Republic of Iran (23), and Yadollahi et al., who related to alcohol consumption in occurrence of RTAs. conducted an epidemiological study of trauma patients who attended national, cultural and religious events Conclusion in the Islamic Republic of Iran (24). Both those studies Trauma is harmful to patients, imposes a burden on the included RTAs and showed that injury in motorcycle healthcare system, and is of significant concern to pub- drivers was more severe than in car drivers. Our study lic health. The findings of our study show that the police was the first to evaluate the risk of accidents caused and law enforcement agencies have a responsibility to ar- by alcohol consumption in Fars Province. The highest range preventive laws to reduce the overall prevalence of prevalence of alcohol consumption among victims of drink driving and decrease the burden of trauma on the RTAs occurred in those aged 20–25 years and it seemed healthcare system. that high-risk behaviour such as alcohol consumption decreased with advancing age. As we indicated, ISS was Funding: This research was supported with grant num- in direct correlation with blood alcohol titre. Our study ber of 97-01-38-16888 by Shiraz University of Medical showed that the percentage of accidents among young Sciences in Shiraz, Islamic Republic of Iran. drinkers was higher than among older patients, which Competing interests: None declared.

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Risque relatif de traumatismes dus à la consommation d'alcool chez les conducteurs de voitures et de motos Résumé Contexte : Il existe des preuves solides indiquant qu'un nombre important de traumatismes, mortels et non mortels, dans les accidents de la circulation résultent de la consommation et de l'abus d'alcool. Objectifs : Examiner la relation entre le taux d'alcoolémie et les caractéristiques des blessures chez les patients traumatisés admis dans un grand hôpital universitaire. Méthodes : Il s'agissait d'une étude transversale des caractéristiques des traumatismes chez 38 435 conducteurs de voitures et de motos envoyés au Centre de traumatologie du sud de la République islamique d’Iran entre octobre et mars 2018. Un modèle de régression log-binomial a été utilisé pour évaluer le risque relatif de chaque covariable en utilisant le Score de gravité des traumatismes. Résultats : 253 patients (7,78 %) avaient une consommation d’alcool. En outre, le taux d'alcoolémie était positif chez 8,66 % et 6,93 % des conducteurs de voitures et de motos, respectivement. Le Score de gravité des traumatismes chez les consommateurs d'alcool et les non-consommateurs était de 6,34 (écart-type ; 8,73) et 4,12 (7,78), respectivement, ce qui était significativement plus élevé chez les consommateurs d'alcool (test t = 12,96, p < 0,001). La consommation d'alcool est donc un facteur important dans l'augmentation du risque relatif de blessure, qui est de 2,83 unités de plus que chez les conducteurs qui n'ont pas consommé d'alcool. Conclusions : Nos conclusions montrent que la police et les forces de l'ordre ont la responsabilité d'appliquer des règles plus strictes pour réduire la conduite sous l’emprise de l’alcool et le fardeau des traumatismes qui pèsent sur le système de soins de santé.

اخلطر النسبي ُّلتعرض سائقي الدراجات النارية والسيارات لإلصابات بسبب تعاطي الكحول مهناز یداهلل، فروغ بجوهیان اخلالصة اخللفية: َث َّمة دالئل قوية عىل أن ًعددا ًكبريا من اإلصابات املميتة وغري املميتة املرتبطة بحوادث املرور عىل الطرق نامجة عن تعاطي الكحول وإساءة استخدامه. األهداف: هدفت هذه الدراسة إىل دراسة العالقة بني تركيز الكحول يف الدم وخصائص اإلصابة لدى مرىض اإلصابات الشديدة الذين ُأدخلوا إىل مستشفى تعليمي رئييس. طرق البحث: ُجري أهذا االستقصاء املقطعي خلصائص اإلصابات الشديدة لدى 38435 سائق سيارة ودراجة نارية ُأحيلوا إىل مركز جنوب إيران لإلصابات الشديدة يف الفرتة بني أكتوبر/ترشين األول ومارس/آذار 2018. ُواستخدم نموذج انحدار لوجستي ذو حدين لتقييم اخلطر النسبي لكل متغري مشرتك عىل درجة وخامة اإلصابة. النتائج: كان هناك 253 مري ًضا )%7.78( يتعاطون الكحول. وكان مستوى الكحول يف الدم إجيابي ًا لدى %8.66 و%6.93 من سائقي السيارات والدراجات الناريةعىل التوايل. وبلغت درجة شدة اإلصابة لدى األشخاص املتعاطني للكحول وغري املتعاطني 6.34)االنحراف املعياري، 8.73( و4.12 ) (عىل 7.78التوايل، وهي أعىل بكثري لدى املتعاطني للكحول )اختبار "يت" = 12.96، الق مةي االحتاملية > 0.001(. ولذا، كان تعاطي الكحول ً عامال ً مهاميف زيادة اخلطر النسبي لإلصابة، والذي زاد لدى السائقني املتعاطني للكحول بواقع 2.83 وحدة ًمقارنة بالسائقني الذين مل يتعاطوا الكحول. االستنتاجات: ُتب ِّني النتائج التي َّتوصلنا إليها أن الرشطة ووكاالت إنفاذ القانون تتحمل مسؤولية إنفاذ قواعد أكثر رصامة للحد من القيادة حتت تأثري تعاطي الكحول، وخفض عبء اإلصابات الشديدة الذي ينوء به نظام الرعاية الصحية.

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Geographic risk of general and abdominal obesity and related determinants in Iranian children and adolescents: CASPIAN-IV Study

Maryam Yazdi,2 Roya Kelishadi,2 Volker Schmid,3 Mohammad-Esmaeil Motlagh,4 Ramin Heshmat 5 and Marjan Mansourian 1

1Pediatric Cardiovascular Research Center, Isfahan Cardiovascular Research Institute, Isfahan University of Medical Sciences, Isfahan, Islamic Re- public of Iran. (Correspondence to: M. Mansourian: [email protected]). 2Child Growth and Development Research Center, Research Insti­tute for Primordial Prevention of Non-Communicable Disease, Isfahan University of Medical Sciences, Isfahan, Islamic Republic of Iran. 3Department of Statistics, Ludwig-Maximilans University, Munich, Germany. 4Department of Pediatrics, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Islamic Republic of Iran. 5Department of Epidemiology, Chronic Diseases Research Center, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran.

Abstract Background: Obesity, as a risk factor for many noncommunicable diseases, is a common public health problem in de- veloped and developing countries. Among Iranian children and adolescents, the prevalence of being overweight has in- creased by almost 50% in the past two decades. Aims: To visualize the geographic differences in general and abdominal obesity risks and related determinants among Iranian children and adolescents. Methods: Participants consisted of 14 880 students, aged 7–19 years, living in urban and rural areas of the Islamic Repub- lic of Iran. Spatial patterns of obesity and its association with related risk factors were identified using Bayesian spatial modeling. Results: The highest spatial risks of general obesity (odds ratio 1.21–1.66 for males and 1.81–2.02 for females) and abdomi- nal obesity (odds ratio 1.20–1.82 for males and 1.25–1.78 for females) were observed in the north, northwest and southwest of the country. Risk of obesity was significantly higher in areas with a higher rate of urban residence, active current smokers and prolonged screen time. Conclusion: Identification of high-risk regions for obesity and spatially related risk factors can be used as informative tools for decision-making and planning in health systems at national and subnational levels. Keywords: geographical mapping, obesity, paediatrics, risk factors, spatial modelling Citation: Yazd M; Kelishadi R; Schmid V; Motlagh M-E; Heshmat R; Mansourian M. Geographic risk of general and abdominal obesity and related de- terminants in Iranian children and adolescents: CASPIAN-IV Study. East Mediterr Health J. 2020;26(12):1532–1538. https://doi.org/10.26719/emhj.20.054 Received: 25/12/18; accepted: 23/09/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction of cardiovascular risk factors revealed a significant correlation between high-body mass index (BMI) clusters Obesity, as a risk factor for many noncommunicable dis- and low socioeconomic status (SES) of the surrounding eases, is a common public health problem in developed community, as well as between elevated BMI and high and developing countries. It has several adverse conse- frequency of smoking in the clustered region (9). quences on different body organs (1). Obesity is one of the most complex clinical disorders in the paediatric age A global overview of obesity indicates a large group (2,3). Among Iranian children and adolescents, the geographic variation in the prevalence rates (13); therefore, prevalence of being overweight has increased by almost knowledge of changes in distribution of obesity helps to 50% in the past two decades. In 2011, 11.9% of Iranian chil- identify populations at risk of future noncommunicable dren and adolescents had general obesity and 19.1% had diseases. However, few studies have assessed the abdominal obesity (4). geographic distribution of general and abdominal obesity Most studies about obesity have focused on (14). BMI has been used frequently in clinical settings determinants of obesity at the individual level. For and population studies in order to assess obesity. BMI is example, any association of obesity with socioeconomics imprecise, but useful for measuring overall adiposity (5). and lifestyle-related variables has been investigated in It has become evident that body fat distribution is also different populations (5–7). However, it would be useful important in predicting obesity-related health risks. It is to recognize how these factors contribute to geographic well known that abdominal obesity is strongly associated variations. Some recent studies have investigated the with cardiovascular and metabolic risks (15). Abdominal association and geographic clustering of obesity risk obesity is mainly investigated using waist circumference factors (8–12). For instance, spatial clustering of obesity (WC), waist-to-hip ratio or weight to height ratio (WHtR) and moderate physical activity attributes have been (1,15–18). Whether these measures should be used to assess investigated at regional levels without considering the obesity-related risks is still unclear. Yan et al. reported relevant determinants (10). In one study, spatial clustering WHtR as an accurate measurement of obesity (18).

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To visualize geographic variation in outcome, mapping Anthropometric measurements is most frequently performed, using an ordinary Poisson In the CASPIAN-IV study, all anthropometric measures or logistic model; however, this approach has some were obtained under standard protocols, using calibrat- disadvantages. This model does not take into account ed instruments. Body weight was measured in light any spatial pattern in outcome; that is, the tendency clothing to the nearest 0.1 kg, and height was recorded for geographically close areas to have similar outcome barefoot, to the nearest 0.1 cm. BMI was calculated as a rates (19). In this regard, considering prior information measure of obesity. WC was measured using a nonelastic on the rates, local geographic dependence could induce tape to the nearest 0.1 cm, at a point midway between the the spatial patterns. Hence, Bayesian estimates of the lower border of the rib cage and the iliac crest at the end rate in an area is shrunk toward a local mean according of normal expiration. The World Health Organization to the rates in the neighbouring areas (20). Also, in this (WHO) growth charts categorize BMI, based on obese modelling framework, covariates as spatial risk factors and nonobese groups (21). Abdominal obesity was also de- can be accounted for by describing variations of rates termined as WHtR > 0.5 (22). between areas. A fully Bayesian approach via Markov Chain Mont Carlo (MCMC) methods is efficient to Covariates assessment estimate prevalence rates and risk of obesity and Students’ information was collected through the stu- modelling-associated risk factors (19,20). dents’ healthcare system. The questionnaires were While the national prevalence rate of different prepared according to the WHO Global School-based types of obesity is an important tool for policy-makers, Student Health Survey (WHO-GSHS). The validity and investigating the distribution of obesity among reliability of the questionnaire had been reported else- geographic areas is equally important for informed where (23). Students completed the questionnaire under decision-making in the allocation of resources for the supervision of healthcare experts. Information was prevention programmes. entered into a checklist by a trained team. The student’ The present study aimed to visualize the geographic parents answered part of the questionnaire. differences in general and abdominal obesity risk Screen time (ST), defined as the hours spent per and prevalence rates, and to determine, using spatial day at weekends and weekdays in watching television modelling, some environmental and socioeconomic risk and using computers, was assessed by the WHO-GSHS factors in a large sample of 7-19-year-old children and questionnaire. The weighted average of ST in a day was adolescents in the Islamic Republic of Iran. The maps obtained by calculating the sum of 1/7 ´ ST on a weekend of general and abdominal obesity were extracted from day and 6/7 ´ ST on a weekday. This weighted average was smoothed spatial odds ratios (ORs), representing spatial divided into quartiles, and the fourth quartile, 4 hours/ obesity risk in different areas of the country, adjusted by day, was considered as prolonged ST. local autocorrelation and uncorrelated heterogeneity. SES was calculated through an approved method in To the best of our knowledge, this is the first and the International Reading Literacy Study (PIRLS) (24). The largest epidemiological study in the Middle East and SES score was calculated, using the principal component North Africa, examining the geographic variation at the analysis (PCA) method based on a questionnaire; asking provincial level, concerning the prevalence rate of general parents about their level of education and occupation, and abdominal obesity in a nationally representative type of school (private or public), type of home (rented or sample of children and adolescents. owned), and family assets (private car and computer). The Methods first tertile of SES score was considered low. Physical activity was assessed by 3 self-report Study population and sampling questions. (1) During the past week, how many days have This study was conducted in 2011 and 2012 as part of a na- you been physically active, for 30 minutes/day? (2) Do you tional school-based project entitled Childhood and Ado- have regular sports classes at school? (3) How much time lescence Surveillance and Prevention of Adult Non-Com- do you spend on regular sports classes at school every municable Disease (CASPIAN-IV) in urban and rural week? A total physical activity score was extracted by areas in different Iranian provinces. The study popula- PCA. The first tertile was considered to be low physical tion consisted of 14 880 school students aged 7-19 years. activity (25). Current smoking status of children and Data were collected in a multistage sampling framework adolescents was also considered as a covariate. in 30 provinces. Stratification was carried out in each Statistical analysis province, according to the area of residence (urban/rural) and school grade (elementary/intermediate/high school). The percentage of obesity and its determinants were The study protocol was approved by the Ethics Commit- calculated and compared between the sexes. Due to sig- tee of Tehran University of Medical Sciences and Isfahan nificant differences between males and females, subse- University of Medical Sciences. After a complete expla- quent analyses were carried out by sex using the c2 test. nation of the study objectives and protocols, written in- To visualize spatial variations in general and abdominal formed consent and verbal consent were obtained from obesity, the Bayesian spatial model represented by Besag, the parents and students, respectively. More details can York and Mollie was used to detect the ORs of obesity in be found elsewhere (4). 30 provincial clusters, compared with the global odds of

1533 Research article EMHJ – Vol. 26 No. 12 – 2020 the whole country (19,20). used (Table 2). According to 95% CIs, in provinces The estimated ORs implied spatial pattern of obesity with significantly higher rates of obesity (general and risk across the regions. In addition, in this modelling abdominal), there was a higher rate of urban residence. approach, the risk factors associated with provincial Urban residence had a stronger impact on the occurrence prevalence rate of general and abdominal obesity were of general obesity in females. Low physical activity did investigated spatially. not show a significant association with any type of obesity. Furthermore, there was no significant association The model was fitted using OpenBUGS version 3.2.2 between high SES and obesity. Abdominal and general (MRC Biostatistics Unit, Cambridge, United Kingdom obesity rates in males had a direct significant association of Great Britain and Northern Ireland). In performing with prolonged ST. Those provinces with higher rates of the MCMC algorithm, each parameter was observed active current smokers had significantly higher rates of to converge within 50 000 iterations of Gibbs sampler, male abdominal obesity. so after discarding the initial 50 000 burn-in values, an To obtain a geographic map of obesity, a mixed additional 20 000 samples were generated for the Bayesian conditional autoregressive model was considered, inference, by choosing the 10th iteration to avoid possible without using covariates. Figures 2 and 3 (online) show autocorrelation. The convergence of model parameters the variation in ORs of general and abdominal obesity was, moreover, evaluated by tracing and autocorrelation in different provinces for males and females. The spatial plots, and Gelman–Rubin criterion. Estimated ORs and ORs were smoothed for spatial autocorrelation and 95% confidence intervals (CIs) for general and abdominal unstructured over dispersion. Spatial risk of abdominal obesity were calculated and shown through geographic and general obesity is geographically varied and there maps, using the map option in GeoBUGS. Statistical were sex differences in the distribution of general and significance was indicated when 95% CIs did not abdominal obesity. include 0. The geographic variation of ORs denoted that the risk Results of general obesity for males and females was higher in the north, northwest, and southwest Iranian provinces, Table 1 shows the prevalence of obesity and related risk compared with the whole country. The provinces with factors in the Islamic Republic of Iran by sex. The rate of the highest ORs for males were Gilan (1.66), Mazandaran general and abdominal obesity in males was 10 and 14%, (1.63), East Azerbaijan (1.54), Qazvin (1.56), Tehran respectively, which was significantly lower than the cor- (1.21), Qom (1.48) and Bushehr (1.29). The provinces responding rate in females (18% and 20%, respectively). with the highest ORs for females were Ardebil (1.81), The rate of obesity-related risk factors, including current East Azerbaijan (1.31), Gilan (1.66), Mazandaran (1.70), smoker and prolonged ST, were significantly higher in Kermanshah (1.32), Bushehr (2.02) and Khuzestan (1.50). males than females (P < 0.05). In contrast, physical activ- The south and southeast provinces had the lowest ORs ity rate in females was significantly less than in males for general obesity in both male and female groups. (P < 0.05). The risk of abdominal obesity was also higher for Figure 1 (online) depicts spatial distribution of females and males in the north, northwest and southwest selected obesity risk factors across the Islamic Republic Iranian provinces, compared with the whole country. of Iran. Urban residence was the dominant lifestyle in The highest ORs for abdominal obesity for males were most provinces. Central provinces, including the capital, in Ardebil (1.82), East Azerbaijan (1.44), Isfahan (1.39), compared to other areas, had the highest rates of low Gilan (1.59), Hamedan (1.27), Kermanshah (1.20), North physical activity, prolonged ST, current smokers and Khorasan (1.34), Markazi (1.30), Mazandaran (1.83), higher SES. Semnan (1.25) and Qazvin (1.33). In females, the highest For evaluating the association of obesity-related ORs occurred in Ardebil (1.52), East Azerbaijan (1.36), risk factors and prevalence rates of obesity in different Qazvin (1.37), Kermanshah (1.25), Gilan (1.28), Golestan geographic areas, the Bayesian spatial regression was (1.42), Mazandaran (1.78), Tehran (1.46) and Bushehr (1.33).

Table 1 Prevalence rates of obesity and related risk factors in males and females aged 7–19 years: the CASPIAN-IV Study Risk factors Female Male P* General obesity 630 (0.10) 859 (0.14) 0.043 Abdominal obesity 1105 (0.18) 1290 (0.20) 0.023 Low physical activity 2440 (0.40) 1816 (0.29) 0.014 Prolonged ST 931 (0.15) 1379 (0.22) <0.001 Current smoking 102 (0.02) 231 (0.04) 0.034 High socioeconomic status 1867 (0.33) 2015 (0.34) 0.143

*χ2 test

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Discussion regression. This discordance might be due to a different age range of their target population and the statistical In this large epidemiological study based on a represent- methods, compared to ours. ative sample of children and adolescents aged 7–19 years in the Islamic Republic of Iran, we investigated using The effect of urban residence on obesity has been the Bayesian spatial model the geographic variation at investigated in some recent national studies in the Islamic the provincial level of the rate of general and abdominal Republic of Iran, for age 7-19 years (7,26,28). Our results obesity. The maps were extracted from smoothed spatial identified the spatially direct association between urban ORs, representing the risk of obesity in different regions residence and obesity in females. Provinces with more according to local autocorrelation and uncorrelated het- urban residents had significantly higher rates of obesity. erogeneity. Both types of obesity had a large geographic Qom, a province in the centre of the country, had the variation. The higher risks of general and abdominal obe- highest number of urban residents, while Hormozgan, in sity were found in the north, northwest and southwest the south, had the lowest number. regions. Possible explanations for this variation are: (1) Smoking is recognized as a critical risk factor for differences in subjects’ characteristics, such as domi- obesity (28,29). Our results demonstrated that abdominal nant lifestyle behaviour, eating habits or dietary patterns, obesity in females was significantly more prevalent in and SES; (2) dissimilarities in healthcare accessibility of provinces with higher rates of active current smokers. different provinces; and (3) differences in health poli- This is in agreement with Chiolero et al. (29) but in cy-making by authorities who support a healthy lifestyle. contrast with Bakhshi et al. (28). Tehran, the capital, had The rate of abdominal obesity was higher than the highest rate of female current smokers. general obesity. The overall rates of both types of obesity In line with previous studies (5,6), our results revealed were higher in males than females, which is in line that prolonged ST was significantly associated with with CASPIAN-IV data from 2003 (26), although the higher rates of abdominal and general obesity among distribution of general and abdominal obesity in males males. and females differed throughout the country. The ethnicity of individuals in this study has been The Bayesian spatial regression model was used to considered, as a part of geographic variations that model the provincial level determinants of obesity in substantially are latent in spatially random parts of the 30 provinces. The risk factors included urban residence, model. One study of Iranian school children indicated low physical activity, active current smokers, low SES that residents of Baluch ethnicity in the southeast had the and prolonged ST. A few studies have investigated the lowest BMI, whereas residents of Turk ethnicity in the determinants of geographic obesity variation (8–11). northwest had the highest BMI, among male children. The current study showed no significant relationship Moreover, Arab female residents in the southwest had between the rate of low physical activity in different the highest BMI (30), which is in line with our extracted areas and obesity, which is in line with the study of maps, based on estimated obesity rates. Schuurman et al. in Vancouver, Canada (10). They found One of the limitations of the current spatial no significant clustering, based on obesity and physical epidemiological study was the occurrence of confounding activity association. However, in contrast to the data bias, which is a common feature in epidemiological obtained by Ford et al. (27) about adults’ obesity-related studies. For example, socioeconomic factors are strong determinants, in 100 metropolitan areas in the United predictors of the majority of health outcomes, but when States of America, we found a significant association exposed to some environmental factors, the confounding between physical activity and obesity rate, using Poisson impact occurs. Lack of many other determinants of obesity,

Table 2 Association of prevalence rates of obesity and risk factors throughout 30 Iranian provinces: the CASPIAN-IV Study Risk factors General obesity Abdominal obesity Male Female Male Female Living in urban area 1.33* 2.76* 1.34* 1.40* (0.46–2.20) (1.65–3.88) (0.43–2.26) (0.32–2.49) Low physical activity 1.20 0.06 3.01 2.81 (5.89 to 8.32) (-10.20 to 10.83) (-4.42 to 10.29) (-5.75 to 11.44) High socioeconomic status 2.78 3.41 5.47 5.39 (3.51 to 9.09) (-4.88 to 11.46) (-0.56 to 11.39) (-0.83 to 11.42) Prolonged ST 10.50* 2.79 10.12* 6.39 (2.04–18.72) (-6.54 to 12.0) (1.87–18.45) (-0.63 to 13.38) Current smoking 2.18 0.73 6.41* 3.14 (3.14 to 7.44) (-3.71 to 5.12) (1.77–11.05) (-0.23 to 6.41)

Regression coefficients and 95% confidence intervals, in Bayesian spatial modelling. * Statistical significance level 0.05.

1535 Research article EMHJ – Vol. 26 No. 12 – 2020 such as major nutritional habits was another limitation spatial autocorrelation and heterogeneity. In the same that could be considered in future investigations. Our modelling framework, we evaluated the spatial impact results were based on information from 30 provinces, in of obesity risk factors. Indeed, environmental and life- which Alborz was considered as part of Tehran; however, style-related risk factors, including urban residence, cur- in the latest country divisions, Alborz was separated rent smoking and prolonged ST were spatially associated from Tehran and there are now 31 provinces. The main with increased risk of obesity in children and adolescents advantages of the current study were using data from a aged 7-19 years. As a result, the spatial Bayesian regres- large population-based survey and providing up-to-date sion model could be effectively used to identify spatial estimates of rates of general and abdominal obesity in 30 risk factors and spatial patterns of obesity. The geograph- Iranian provinces. Longitudinal studies are suggested for ic mapping of high-risk regions for general and abdomi- determining the trends in general and abdominal obesity, nal obesity presented could be useful for decision-mak- and examining precise determinants that can be useful ing and planning in health systems. A high incidence for health policy-makers. rate of obesity-related disorders is expected in the future, imposing a considerable economic burden on the health Conclusion system; therefore, identifying high-risk regions, spatial We estimated the rates of abdominal and general obesity, pattern of obesity and the spatial risk factors could be and specified the local risk of obesity across Iranian prov- applied to epidemiological prediction and optimal alloca- inces, using a spatial Bayesian model that considered tion of health resources among different regions.

Acknowledgement This nationwide survey was conducted in Iran with the cooperation of the Ministry of Health and Medical Education; Ministry of Education and Training, Child Growth and Development Research Center, Isfahan University of Medical Sciences; and Endocrinology and Metabolism Research Center of Tehran University of Medical Sciences. Funding: None. Competing interests: None declared.

Risque géographique lié à l’obésité générale et abdominale et ses facteurs déterminants chez les enfants et les adolescents iraniens : l’étude CASPIAN-IV Résumé Contexte : L'obésité, en tant que facteur de risque de nombreuses maladies non transmissibles est un problème de santé publique courant dans les pays développés et en développement. La prévalence du surpoids chez les enfants et les adolescents iraniens a augmenté de près de 50 % au cours des deux dernières décennies. Objectifs : Visualiser les différences géographiques dans les risques d'obésité générale et abdominale et les déterminants connexes chez les enfants et les adolescents iraniens. Méthodes : Les participants se composaient de 14 880 élèves et étudiants, âgés de 7 à 19 ans, vivant dans les zones urbaines et rurales de la République islamique d'Iran. Les schémas spatiaux de l'obésité et son association avec des facteurs de risque connexes ont été identifiés à l'aide d'une modélisation spatiale bayésienne. Résultats : Les risques spatiaux les plus élevés d'obésité générale (odds ratio 1,21-1,66 pour les hommes et de 1,81-2,02 pour les femmes) et d'obésité abdominale (odds ratio 1,20-1,82 pour les hommes et 1,25-1,78 pour les femmes) ont été observés dans le nord, le nord-ouest et le sud-ouest du pays. Le risque d'obésité était significativement plus important dans les zones à forte densité urbaine, où le nombre des fumeurs actifs est plus élevé et où le temps passé devant un écran est plus long. Conclusion : L’identification des régions à haut risque d'obésité et des facteurs de risque ayant une association spatiale peut être utilisée comme outils d'information pour la planification et la prise de décision au sein des systèmes de santé aux niveaux national et infranational.

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اخلطر اجلغرايف لإلصابة بالسمنة العامة وسمنة البطن ُوامل ِّ دات حدوثيقة الصلة لدى األطفال واملراهقني اإليرانيني: دراسة CASPIAN-IV مريم يزدى، رويا كليشادي، فولكر شميد، حممد إسامعيل متالغ، رامني حشمت، مرجان مانسوريان اخلالصة اخللفية: ُتعد السمنة، باعتبارها عامل خطر للعديد من األمراض غري السارية، أحد مشاكل الصحة العامة الشائعة يف البلدان املتقدمة والنامية. وقد زاد معدل انتشار زيادة الوزن بني األطفال واملراهقني اإليرانيني بنسبة %50 ًتقريبا خالل َالعقد ْني َاملاضي ْني. هدفت األهداف:هذه الدراسة إىل توضيح االختالفات اجلغرافية يف خماطر السمنة العامة وسمنة البطن ُوامل ِّحددات وثيقة الصلة بني األطفال واملراهقني اإليرانيني. طرق البحث: َّفتأل املشاركون من 14880 ًطالبا، ترتاوح أعامرهم بني 7 سنوات و سنة، 19يعيشون يف املناطق احلرضية والريفية يف مجهورية إيران اإلسالمية. ُوح ِّددت األنامط املكانية للسمنة، وارتباطها بعوامل اخلطر وثيقة الصلة باستخدام نامذج بايز املكانية. النتائج: لوحظت أعىل املخاطر املكانية للسمنة العامة )حيث تراوحت نسبة األرجحية لإلناث من 1.21إىل 1.66، وللذكور من 1.81إىل 2.02( ولسمنة البطن )حيث تراوحت نسبة األرجحية من 1.25 إىل 1.78لإلناث، و 1.20 إىل 1.82 للذكور( يف الشامل والشامل الغريب واجلنوب الغريبمن البلد. وارتفع خطر اإلصابة بالسمنة بكثري يف املناطق التي ترتفع فيها معدالت اإلقامة يف املناطق احلرضية، واملدخنون احلاليون النشطون، ومعدالت قضاء وقت طويل أمام الشاشات. االستنتاجات:يمكن االستفادة من حتديد املناطق ذات اخلطر املرتفع لإلصابة بالسمنة، وعوامل اخلطر املرتبطة هبا ًمكانيا كأدوات ُي َسرتشد هبا يف اختاذ القرارات والتخطيط يف ُّالنظم الصحية عىل َالصعيد ْين الوطني ودون الوطني.

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Views of community pharmacists in Lebanon on the unified prescription: a mixed method study

Hani Dimassi,1 Aline Bou Maroun,2 Marguerita Saadeh,3 Joanne Khabsa,2 Jessica-Lynn Abdou 2 and Shadi Saleh 4

1Department of Pharmaceutical Sciences, School of Pharmacy, Lebanese American University, Byblos, Lebanon. 2Department of Pharmacy Practice, School of Pharmacy, Lebanese American University, Byblos, Lebanon. 3Karolinska Institutet and Stockholm University, Stockholm, Sweden. 4Depart- ment of Health Management and Policy, American University of Beirut, Beirut, Lebanon. (Correspondence to: Hani Dimassi: [email protected]).

Abstract Background: The unified prescription was introduced in Lebanon in 2011; an aim was to save on medication expenditure. Aims: The aim of this study was to evaluate the views of community pharmacists on the effect and usefulness of the unified prescription. Methods: A cross-sectional telephone survey of community pharmacists from all governorates of Lebanon was conduct- ed. A questionnaire was used to collect demographic data, pharmacists’ views on the effect of the unified prescription on their work, the percentage of prescriptions in which the prescriber had indicated that the medicine should not be substi- tuted with a generic equivalent and the percentage needing clarification from the prescriber. Face-to-face interviews were held with 12 pharmacists to explore their views further. Results: Of 251 pharmacists interviewed, 56.8% did not think the unified prescription was useful, 34.8% thought it compli- cated their work and 24.0% that it reduced their autonomy. The in-depth interviews showed that autonomy was perceived to be restricted because of the difficulty in convincing patients to accept a substitute generic medicine, which the unified prescription allowed. The unified prescription complicated pharmacists’ work because of increased paperwork and the need for more storage. Pharmacists felt that the large number of prescriptions in which the prescriber had indicated that the medicine should not be substituted undermined the purpose of the unified prescription. Conclusion: The implementation of the unified prescription was not considered a success by community pharmacists in Lebanon. Efforts are needed to improve communication with prescribers and educate the public about pharmacists’ role and generic medicines. Keywords: pharmacists, prescriptions, drugs, generics, Lebanon Citation: Dimassi H; Maroun AB; Saadeh M; Khabsa J; Abdou J; Saleh S. Views of community pharmacists in Lebanon on the unified prescription: a mixed method study. East Mediterr Health J. 2020;26(12):1539–1547. https://doi.org/10.26719/emhj.20.127 Received: 30/10/19; accepted: 15/03/20 Copyright © World Health Organization (WHO) 2020. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https:// creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction (1,2). The triplicate prescription allows the monitoring of prescribing practices, provides feedback on targeted In 2011, a new unified prescription was introduced in Leb- drugs and identifies areas of misuse (3). anon, as a result of which the pharmacy profession had to make some substantial changes to their practices. This The Lebanese government’s intention with the unified new policy was designed to improve health care services, prescription programme was to reduce medication costs by increasing the use of cheaper generic medicines. The in which pharmacists play an important role; however, no programme would empower pharmacists to suggest studies have evaluated the effect of the unified prescrip- substitution to their clientele who were presenting tion on the daily practice of community pharmacists and prescriptions to be filled(4) . Relieving the burden on whether they were able to adapt to the changes. public finances is essential, particularly as expenditure The triplicate prescription form was instated by on prescription drugs in Lebanon is estimated to rise to ministerial decision no. 1925 issued by the Lebanese US$ 2.71 billion in 2020, accounting for 52% of total health government in 2011. This decision introduced the unified expenditure (4). prescription form with three copies: white for the patient, With generic substitution at the core of the unified pink for the pharmacist and yellow for the physician. Its prescription programme, pharmacists are supposed to objective differed from that of the triplicate prescription play a key role in addressing patients’ enquiries about programme in North America. generic drugs and correcting any misconceptions on Triplicate prescription forms have been used in their effectiveness and value (5,6). The usually lower cost the United States of America (USA), Canada and other of generic medicines is often mistakenly interpreted as countries to monitor certain drugs with high potential inferiority of these medicines compared with proprietary for abuse. For instance, in 1989, New York State medicines with known brand names. This obstacle for mandated triplicate prescription for benzodiazepines substitution is more obvious with lower educational

1539 Research article EMHJ – Vol. 26 No. 12 – 2020 level and socioeconomic status of patients (7–9). As such, (ii) that required an intervention from the pharmacist. pharmacists are in a unique position to educate patients We developed the questionnaire in English and two inde- about bioequivalence studies and good manufacturing pendent professional translators translated it into Arabic practices that generic medicines undergo to overcome and then back-translated it for validation; there were no any mistrust patients may have about accepting drug major discrepancies between the translators. Finally, we substitution (9,10). pilot-tested the questionnaire on community pharma- The implementation of the unified prescription was cists who were not included in the final sample for clarity expected to affect the physician–pharmacist–patient and appropriateness of questions, as well as the length of relationship, especially the pharmacists who are the link the interview. between the prescriber, the patient and the medication. The in-depth interview was based on three areas Therefore, the aim of our study was to evaluate the views of discussion: (i) How do you define autonomy in of community pharmacists on the newly implemented your pharmacy practice?; (ii) How did the new unified unified prescription in terms of its usefulness and its prescription affect your work?; and (iii) How useful has effect on their workflow – its complexity and their the unified prescription been? autonomy. Pharmacists’ autonomy is their ability to do their jobs independently without having to refer Data collection to physicians for drug substitutions, and to make and Two pharmacy graduates collected the data for phase 1 implement decisions for the benefit of the patient. over the phone. They were trained on how to remain objective, how to probe and how to prevent divergence Methods from the questions. All respondents gave verbal consent Design and sample to participate. In case of refusal or a wrong number, we randomly selected a replacement from the same governo- This was a mixed-method study: the first part (phase 1, rate. We gave the respondents the option to be called later June–August 2016) was a quantitative survey and the sec- at a more convenient time. ond part was qualitative interviews (phase 2, April 2017). Phase 1 was a national cross-sectional survey of commu- In the second phase, all 12 pharmacists who nity pharmacists working in Lebanon. A complete list of participated in the face-to-face in-depth interview these pharmacists was extracted from the directory of the provided their consent. We interviewed these Order of Pharmacists of Lebanon, which included also pharmacists at their pharmacies. The interviews were the pharmacy’s name, telephone number and address. audio-recorded and tapes were reviewed for data analysis The list was stratified by the six Lebanese governorates and theme identification. and a stratified random sample proportionate to size was Data analysis selected. The targeted sample size was 300 pharmacists based on a 95% confidence interval with 5–6% precision. The interviewers used Excel for data entry of the data To reach the target sample size of 300, we attempted to collected during the telephone survey using a coding contact 463 pharmacists, of whom 161 either declined to scheme. The final data entry sheet was imported toSPSS , participate, the telephone number was wrong, or there version 24 (12). We used frequencies and percentages to was no answer, giving a response rate to 65.2%. Further- summarize categorical variables, and means and stand- more, we excluded 51 participants because they did not ard deviations (SD) to summarize numerical variables. hold a pharmacy degree, so the final sample size was We used the Pearson chi-squared test and the ANOVA F 251. Phase 2 was an in-depth face-to-face interview with test to assess differences in proportions and means, re- 12 pharmacists from the six governorates, representing spectively. We set the level of significant atP ≤ 0.05. both sexes and employment status (owner versus em- We reviewed and analysed the audio recordings and ployee). This sample proved to be sufficient as data satu- notes taken during the face-to-face interview to identify ration was reached (11). the themes that emerged. Questionnaire Ethical considerations The questionnaire included different sections: demo- This study was approved by the Institutional Review graphic data of the pharmacists, views of the unified Board of the Lebanese American University (LAU.SOP. prescription. The demographic section included ques- HD2.0/Jul/2016), and amended for face-to-face interviews tions about age, sex, years of experience, degree (BSc in (LAU.SOP.HD2.5/Jul/2016). Oral consent was obtained pharmacy versus PharmD) and ownership of the phar- from the participants for the telephone and the face-to macy (versus employee) (independent variables). The fact interviews. unified prescription section asked three questions: was the unified prescription useful, did it affect work auton- Results omy and did it affect the workflow (did it make it more complicated or simpler). The last section were questions Results from the telephone survey about the percentage of prescriptions: (i) in which the The sample represented all six Lebanese governorates prescriber had indicated that no substitution of the pre- with a distribution that closely matched the distribution scribed medicine should be made by the pharmacist and of community pharmacies in the country. Males (51.8%)

1540 Research article EMHJ – Vol. 26 No. 12 – 2020 and females (48.2%) were almost equally represented and Table 1 Characteristics of community pharmacists, Lebanon the biggest proportion were aged 30–39 years (35.2%). Characteristic No. % Most of the pharmacist had a bachelor of science degree (n= 251) (61.4%) compared with 38.6% with a degree in pharmacy, Governorate 80.1% were pharmacy owners and 74.8% had more than 6 years of experience (Table 1). Beirut 26 10.4 Bekaa 35 13.9 More than half of the pharmacists (56.8%) did not think that the unified prescription was useful, and Mount Lebanon 122 48.6 48.8% did not think it had affected their workflow Nabatieh 13 5.2 (neither simplifying nor complicating it) and 63.2% did North 33 13.1 not think it had affected their autonomy. Nonetheless, South 22 8.8 of the remaining 128 pharmacists, most perceived Sex a negative impact: 68% of the 128 reported that the unified prescription complicated their work (rather than Male 130 51.8 simplified it), and 65% reported that it reduced their Female 121 48.2 autonomy (rather than increased it). Age group (years) Pharmacists reported an average of 59.8% (median 20–29 62 25.1 70%) of prescriptions were labelled with no substitution 30–39 87 35.2 by the prescribing physician. Furthermore, they reported 40–49 57 23.1 an average of 23.7% prescriptions needed further 50–77 41 16.6 clarification from the prescribing physician, mostly because of unclear handwriting (92.4%), followed by Missing 4 wrong dose (45.0%) (Table 2). Degree Responses to the three unified prescription questions BSc in pharmacy 154 61.4 were statistically associated. Pharmacists who perceived PharmD 97 38.6 the unified prescription to be useful, compared to Position not useful, were more likely to report that unified Pharmacy owner 201 80.1 prescription simplified their work (36.4% versus 1.4%, Pharmacy employee 50 19.9 P < 0.001), and increased their autonomy (23.4% versus 4.9%, P < 0.001) (Table 3). In addition, those claiming that Years of experience unified prescription increased their autonomy were more ≤ 5 63 25.3 likely to report it simplified their work as well (56.3% 6–15 96 38.6 versus 10.0% among those that reported less autonomy, ≥ 16 90 36.1 P < 0.001; Table 4). Missing 2 Results of a bivariate analysis comparing responses to the three questions on the unified prescription across the independent variables in the study failed to detect any significant differences, indicating that the pharmacists’ the previous year, making generic substitution no longer answers to the unified prescription questions were meaningful. As one pharmacist explained: “Unified pre- uniform across their socioeconomic backgrounds. scription was meant to decrease costs through gener- Therefore, we decided to carry out in-depth interviews ic substitution; whereas currently, some generics are with a group of pharmacists to further understand their more expensive than brands” (female, Beirut, employee). viewpoint. On the other hand, a few pharmacists thought that the Results of the qualitative analysis unified prescription added to their autonomy: “Unified prescription provided autonomy by giving us the ability When we asked the pharmacists interviewed about how they defined work autonomy, they pointed to the abili- and authorization to substitute brand for generic” (male, ty to do their jobs independently, without having to re- Mount Lebanon, owner). Another pharmacist described fer to physicians for drug substitutions, and the ability the actual situation: “Theoretically, the unified prescrip- to make and implement decisions for the benefit of the tion was supposed to give more autonomy to pharma- patient. When we asked how their autonomy was linked cists, however, it did not, since the list of substitutes is to the unified prescription, most pharmacists said that it not clear nor readily accessible, and doctors are using ‘no did not add to their autonomy. “Autonomy was restrict- substitution’ excessively” (female, North, owner). A fe- ed by unified prescription, either because of no substi- male pharmacy owner in South governorate raised a con- tution use or because generics are more expensive than cern shared by other pharmacists: “When no substitution brands” (male, Mount Lebanon, owner). In fact, most of is not recorded on the prescription, we have trouble con- the pharmacists we interviewed brought up the lack of vincing patients of the substitution without calling the an adequate pricing strategy. They reported that the price physician. They obviously trust their doctors much more of brand medications had decreased substantially over than they trust us.”

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Table 2 Views of community pharmacists on the unified prescription, Lebanon Question No. (n = 250) % Is the unified prescription helpful? Yes 108 43.2 No 142 56.8 Missing 1 Did the unified prescription simplify or complicate your work? Simplified 41 16.4 Complicated 87 34.8 No change 122 48.8 Missing 1 How did the unified prescription affect your autonomy? Less autonomy 60 24.0 More autonomy 32 12.8 Did not change 158 63.2 Missing 1 Percent of prescriptions: Mean (SD) Median (IQR) Labelled as non-substitutable a 59.8 (28.2) 70 (38.7) Needed clarification from prescriber 23.7 (24.5) 15 (35.0) Problem encountered with prescriptions No. (n = 251) % Wrong dose 113 45.0 Drug–drug interaction 68 27.1 Wrong dosage form 60 23.9 Drug–disease interaction 53 21.1 Wrong drug 47 18.7 Unclear handwriting 232 92.4

SD: standard deviation; IQR: interquartile range. aThe doctor indicates on the prescription that the brand medicine should not be replaced by the pharmacist with an equivalent generic medicine.

When we asked the pharmacists if the unified form, otherwise, we will lose customers” (female, Mount prescription had simplified or complicated their work, Lebanon, employee). Therefore, a commonly reported most complained that it complicated their daily tasks. It concern of pharmacists was reinforcing the use of the added to their paperwork and increased the storage space unified prescription among all physicians. Interviewees required. The pink copy of the prescription, which is to be reported that a large number of prescriptions are marked kept at the pharmacy, is hard to read, of poor quality and with no substitution, even when the prescription is for the ink fades with time. As explained by one pharmacist: a generic medicine, indicating that doctors may lack an “The pink copy is worthless after a few months because understanding of the purpose of no substitution or are the ink disappears” (male, Mount Lebanon, owner). “It is receiving remuneration from companies to write no not clear how long we should keep the prescription forms, substitution. and they are taking significant storage space” (male, A shared idea among pharmacists was that: “Unified Mount Lebanon, owner), Another pharmacist said: “Pink prescription could have been more useful if it involved copies are almost never stamped, and when it comes to a change in the health care strategy, introduction of a prescriptions for controlled substances, we have to send patient profile system and electronic prescribing” (male, the patient back to the doctor’s office to have it stamped, Mount Lebanon, owner). However, one pharmacist was otherwise, it is not valid for dispensing” (female, South, a little more optimistic: “Unified prescription is partially owner). useful. We are on the right track, but it has to be part of As for the usefulness of the unified prescription, a whole system change” (male, North, owner). Additional the interviewees stated that, although the form used is reported barriers to effective implementation of the professional, well divided and user-friendly, it is not of unified prescription included lack of patient awareness added value. They stated that doctors do not fully abide about generic medicines and little trust in community by the form. Pharmacists still receive old prescription pharmacists: “I have to call the physician so that he/ forms, especially for non-Lebanese patients and patients she convinces the patient of the proposed swap [to a without third-party coverage. One pharmacist stated: generic medicine]” (female, Mount Lebanon, employee). “We should dispense the drug despite the use of the old Similarly, another pharmacist explained that he rarely

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Table 3 Perception of community pharmacists of the usefulness of the unified prescription and its effect on their work and autonomy, Lebanon Effect of unified prescription on: Unified prescription perceived as: P-value Useful (n = 107) Not useful (n = 142) No. % No. % Work < 0.001 Less complicated 39 36.4 2 1.4 More complicated 21 19.6 65 45.8 No change 47 43.9 75 52.8 Autonomy < 0.001 Less autonomy 27 25.2 33 23.2 More autonomy 25 23.4 7 4.9 No change 55 51.4 102 71.8

bothers to offer a substitute: “It is a waste of energy to override. However, implementation of the new form is try to explain to the patient that I am only offering an still incomplete which may explain the mixed reactions equivalent drug. I have had several patients who came of the community pharmacists surveyed. The main back after purchasing the generic to exchange it for the problems reported were related to generic substitution, initially prescribed drug” (male, Mount Lebanon, owner). unclear guidance on implementation of the new form Other pharmacists commented: “A whole population and lack of public education about generic drugs and the attitude needs to be changed through education, role of a community pharmacist. including education about the role of the pharmacist” Generic medicines are often considered by health (male, Mount Lebanon, owner), and “We are not allowed care professionals as inferior to their brand counterparts, to exert our role as drug experts, and that needs a national mainly because of a sense of lack of compliance with awareness campaign” (female, Beirut, employee). the good manufacturing practices (14). Our findings that a large number of physicians frequently use the no Discussion substitution option concur with previous studies (15,16). In this study, we tried to examine the effect of introduc- Possible explanations could be the poor trust of physicians ing the new unified prescription, 5 years after its launch in generic drugs as well as promotional incentives by the Lebanese government. In response to this new given to them by pharmaceutical companies. A review procedure, we found that the majority of Lebanese phar- of physicians’ perceptions on proprietary medicine macists had a negative opinion of the introduction of the concluded that the poor knowledge of physicians about unified prescription. biosimilar generic medicines was the main reason for such practice (17). A study in Jordan showed that 50– The new unified prescription form is available in 80% of physicians in Jordan were likely to oppose the three colour-coded copies: white for the patient (primarily replacement of brand drugs with generic substitutes (18). for third party payer reimbursement), pink for the Another study from the United Arab Emirates showed pharmacist (as a record of dispensing) and yellow for the that only 17% of patients were prescribed a generic drug physician (as proof of prescribing). The main difference and 56% received no background information from their from the previously used prescription form was the physician about the availability of a generic medicine (19). introduction of the generic substitution which allowed Furthermore, a Danish study highlighted the importance pharmacist to dispense an equivalent generic medicine of removing incentives to use branded drugs as a way to rather than the proprietary branded one indicated by the increase prescription of generic medicines (20). In spite doctor. Nonetheless the authority of the physician was of a documented surge in pricing of generic medicines maintained as he/she could select the non-substitutable across the world because, for example, drug shortages, medication option as per article 47 of the law of practice supply disruptions and consolidations in the generic- of pharmacy profession (13), which the pharmacist cannot drug industry, they are still the cheaper option (21,22).

Table 4 Effect of the unified prescription on the autonomy of community pharmacists and the complexity of their work, Lebanon Effect on work complexity Less autonomy (n = 60) More autonomy (n = 32) No change (n = 157) P-value No. % No. % No. % Less complicated 6 10.0 18 56.3 16 10.2 < 0.001 More complicated 29 48.3 3 9.4 55 35.0 No change 25 41.7 11 34.4 86 54.8

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In fact, decreasing the health care cost for both patients The 2017 Lebanese study also supported the need for and governmental agencies was and remains the main raising awareness about generic drugs among the public objective of the unified prescription. However, a unique (15). For instance, discussing monetary concerns with cost reduction policy that came into effect in Lebanon in patients might be a good start for the pharmacists to 2015 (23) resulted in substantial decrease in the price of highlight the financial value of generics while correcting brand name medicines, which counteracted the financial any common false beliefs that they may have about those benefit of many generic substitutions. drugs (10). Pharmacists reported a collective sense that the A different but related issue is the low public trust in execution of the unified prescription was ill-prepared, a community pharmacists. Pharmacists are the experts in finding supported by a 2017 study which reported a lack medicines and their role extends far beyond dispensing; of adequate infrastructure and no clear direction on how they frequently have to intervene to correct prescription to use the forms (16). Pharmacists were unsure of how errors (30). Educating and raising awareness among long they should keep the pink copies or how they should the public about the role that pharmacists in product file them while pointing out to the poor ink quality, a problem that has been previously raised (24). Moreover, selection is needed. physicians continue to use the old form, especially for In light of these issues, we recommend that efforts uninsured or non-Lebanese patients, and pharmacists are made by the government to raise awareness among find themselves obliged to fill the prescription. the public that brand medicines can be changed for their A study in Denmark listed a number of difficulties generic equivalent and to help them understand that facing the implementation of a new prescription policy, generic medicines are a cost-saving option with the same including insufficient knowledge of physicians and efficacy as their brand counterparts. The government uncertainty about procedures, unclear responsibilities, should also work alongside pharmacists to highlight insufficient communication, clinician autonomy and these issues and come up with solutions that will low acceptance of the change (25). Pharmacists surveyed improve the unified prescription and support the role of reported on average a 1-hour increase in workload per pharmacists in providing the best patient care. day, while most physicians stated that they did not A limitation of our study is that it focused on how the fully understand all parts of the form. Overall, both unified prescription affected the work of pharmacists and pharmacists and physicians were dissatisfied with the overlooked the perspectives of patients and physicians. new system (26). Taking account of the views of all involved parties on the Lebanese pharmacists believed that the unified prescription process could allow a better understanding prescription could have been more meaningful if it had of the issue at hand. Another limitation is the possibility been part of a larger national drug policy change. Such of measurement bias. Perceptions and views are indirect an initiative could include implementation of patient measures and cannot substitute for direct measures. profiles, electronic pharmacy records and electronic However, direct measurement of usefulness and prescribing, and a clear list of over-the-counter medicines. workflow is hard to undertake. Studies confirm that electronic prescribing has a positive effect on the safety of prescribing practices (26) and can Notwithstanding these limitations, our study used a eliminate transcription errors (27). In theory, a modified mixed-method approach where the qualitative data along prescription form that requires relevant medication with the quantitative data provided a more comprehensive information would reduce prescribing problems (28). understanding of the issues with the unified prescription Pharmacists lacked the motive to dispense generic and a clearer insight of pharmacists’ perceptions of this medicines because of poor incentives, lower profit and problem. Furthermore, to our knowledge, this is the first patients’ resistance to change. According to a 2017 study, national study, whereby the results are representative of more than half of the Lebanese population is not aware all Lebanese community pharmacists. of a definition of a generic drug and a larger proportion Funding: Lebanese American University – School of (68%) is not sure of the pharmacological equivalency of Pharmacy; grant number LAU SOP 2016-16. The funding the generic drug (15). Patients have constantly shown body did not play any role in the study design, data collec- poor acceptance of substitution and insistence on the tion or interpretation. The fund provided was used to pay drug selected by the doctor. This is in contrast to the interviewers’ salaries. USA where the generic drug is widely prescribed (22), accounting for about 86% of all filled prescriptions (29). Competing interests: None declared.

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Points de vue des pharmaciens d'officine au Liban sur la prescription unifiée : une étude à méthodologie mixte Résumé Contexte : La prescription unifiée a été introduite au Liban en 2011. L’objectif était d’économiser sur les dépenses de médicaments. Objectifs : L’objectif de cette étude était d’évaluer le point de vue des pharmaciens d’officine sur l’effet et l’utilité de la prescription unifiée. Méthodes : Une enquête téléphonique transversale a été menée auprès des pharmaciens d’officine issus de tous les gouvernorats du Liban. Un questionnaire a été utilisé pour recueillir des données démographiques, le point de vue des pharmaciens en ce qui concerne l'effet de la prescription unifiée sur leur travail. Il a également permis de recueillir le pourcentage de prescriptions pour lesquelles le prescripteur avait indiqué que le médicament ne devait pas être remplacé par un équivalent générique et le pourcentage nécessitant une clarification de la part du prescripteur. Des entretiens en face à face ont eu lieu avec 12 pharmaciens pour étudier leurs points de vue. Résultats : Sur 251 pharmaciens interrogés, 56,8 % ne pensaient pas que la prescription unifiée fût utile, 34,8 % trouvaient que cela compliquait leur travail et 24,0 % estimaient qu’elle réduisait leur autonomie. Les entretiens approfondis ont montré que l’autonomie était considérée comme limitée en raison de la difficulté à convaincre les patients d’accepter un médicament générique de substitution, ce que la prescription unifiée permettait. Ce type de prescription a compliqué le travail des pharmaciens en raison des formalités accrues et de la nécessité de disposer de davantage de stockage. Les pharmaciens estimaient que le grand nombre de prescriptions dans lesquelles le prescripteur avait indiqué que le médicament ne devait pas être substitué compromettait l'objectif de la prescription unifiée. Conclusions : La mise en place de la prescription unifiée n’a pas été considérée comme un succès par les pharmaciens d’officine au Liban. Des efforts doivent être consentis pour améliorer la communication avec les prescripteurs et sensibiliser le public au rôle que jouent les pharmaciens et les médicaments génériques.

آراء الصيادلة املجتمعيني يف لبنان بشأن الوصفة الطبية ّاملوحدة: دراسة قائمة عىل مزيج من األساليب هاين دياميس، الني بو مارون، مارجريتا سعادة، جوان خبصا، جسيكا-لني عبده، شادي صالح اخلالصة اخللفية: ُأدخلت الوصفة الطبية ّ دةاملوح يف لبنان يف عام 2011. َوت ّثل أحد أهدافها يف التوفري يف نفقات األدوية. األهداف:هدفت هذه الدراسة إىل تقييم آراء الصيادلة املجتمعيني بشأن التأثري املرتتب عىل الوصفة الطبية ّاملوحدة وفائدهتا. طرق البحث: ُأجري مسح هاتفي مقطعي للصيادلة املجتمعيني من مجيع حمافظات لبنان. ُواستخدم استبيان جلمع بيانات سكانية وآراء الصيادلة بشأن تأثري الوصفة ّاملوحدة عىل عملهم، ونسبة الوصفات الطبية التي أشار فيها واصفوها إىل رضورة عدم استبدال الدواء بام يكافئه من األدوية اجلنيسة والنسبة املئوية التي حتتاج إىل توضيح من واصف الوصفة الطبية. ُوعقدت مقابالت ًوجها لوجه مع 12 ً صيدلياللتعرف عىل آرائهم بشكل أكرب. النتائج:من بني 251 ًصيدليا ُأ َتجري مقابالت معهم، رأى %56.8منهم أن الوصفة الطبية ّاملوحدة مفيدة، ورأى %34.8 أهنا قد ّتأد إىل جعل عملهم أكثر ًتعقيدا، ورأى %24.0 منهم أهنا خفضت من استقالليتهم. وأظهرت املقابالت ُاملتعمقة أن الصيادلة رأوا أن استقالليتهم باتت حمددة بسبب صعوبة إقناع املرىض بقبول أحد األدوية اجلنيسة املكافئة، وهو األمر الذي سمحت به الوصفة الطبية ّاملوحدة. وقد ّأدت الوصفة الطبية ّاملوحدةإىل تعقد عمل الصيادلة ألهنا أدت إىل زيادة حجم العمل الورقي واحلاجة إىل مساحة أكرب للتخزين. وقد رأى الصيادلة أنه قد حدث تقويض للغرض من الوصفة الطبية ّاملوحدة بسبب العدد الكبري من الوصفات الطبية التي أشار فيها واصفوها إىل رضورة عدم استبدال الدواء. االستنتاجات:رأى الصيادلة العاملون يف الصيدليات يف لبنان أن تنفيذ الوصفة الطبية ّاملوحدة مل حيالفه النجاح. وهناك حاجة إىل بذل جهود لتحسني االتصال ُبم ّقدمي الوصفات الطبية وتثقيف اجلمهور بشأن دور الصيادلة واألدوية اجلنيسة.

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Identification of immunoreactive proteins in secretions of Leishmania infantum promastigotes: an immunoproteomic approach

Sajad Rashidi,1 Paul Nguewa,2 Zahra Mojtahedi,3,4 Bahador Shahriari,5 Kurosh Kalantar 6 and Gholamreza Hatam5

1Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 2Department of Microbiology and Parasitology, ISTUN Instituto de Salud Tropical, University of Navarra, Pamplona, Spain. 3Institute for Cancer Research, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 4Department of Health Care Administration and Policy, School of Public Health, Uni- versity of Nevada, Las Vegas, Nevada, United States of America. 5Basic Sciences in Infectious Diseases Research Center, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 6Department of Immunology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. (Correspondence to: Gholamreza Hatam: [email protected], and Paul Nguewa: [email protected]).

Abstract Background: In the Mediterranean region, Leishmania infantum is the main cause of visceral leishmaniasis. Dogs with ca- nine visceral leishmaniasis are an important reservoir of visceral leishmaniasis. Control of canine visceral leishmaniasis could disrupt transmission of visceral leishmaniasis to humans. The secreted antigens of Leishmania promastigotes are potential stimuli of the host immune system. Proteomic techniques facilitate the identification of new protein markers. Aims: This study aimed to identify immunoreactive proteins in the secretions of L. infantum promastigotes which could be possible targets for the diagnosis and treatment of canine visceral leishmaniasis and the development of vaccines against the disease. Methods: Secretions of L. infantum promastigotes were obtained from the cultivation of 6 × 109 promastigotes in se- rum-free RPMI-1640 medium during a period of 72 h. After deionization and lyophilization, two-dimensional gel electro- phoresis was used for protein separation followed by Western blotting. Thirteen common and repeatable immunoreactive spots were analysed by mass spectrometry. Results: Nine proteins were identified by spectrometry. Most of these proteins were involved in metabolism pathways, survival and pathogenicity of Leishmania parasites. Phospholipase C, immune inhibitor A, chitin-binding protein and a single peptide match to chain A crystal structure of selenomethionine were observed in the secretions of L. infantum pro- mastigotes. Conclusions: The proteins identified in metabolism pathways, survival and pathogenicity of Leishmania parasites are possible targets that could be used for the diagnosis and treatment of canine visceral leishmaniasis and the development of vaccines against the disease in the future. Keywords: visceral leishmaniasis, Leishmania infantum, dogs, proteomics, mass spectrometry Citation: Rashidi S; Nguewa P; Mojtahedi Z; Shahriari B; Kalantar K; Hatam G. Identification of immunoreactive proteins in secretions of Leishmania infantum promastigotes: an immunoproteomic approach. East Mediterr Health J. 2020;26(12):1548–1555. https://doi.org/10.26719/emhj.20.114 Received: 24/09/19; accepted: 09/03/20 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction Proteomic techniques can show the proteome profile of cells and biological fluids and can also provide more Visceral leishmaniasis (VL) is the severe form of a group information on protein functions and post-translational of diseases caused by Leishmania donovani complex. In VL, modifications of proteins(5) . The application of mass the reticuloendothelial system is invaded by these para- spectrometry and proteomic techniques in the laboratory sites. L. infantum is the main cause of VL in the Mediterra- and in the identification of therapeutic targets has been nean region. The prevalence of VL is high in endemic ar- reported in the past decade (6–9). Furthermore, proteomic eas such as the Indian subcontinent and south-west Asia techniques have received more attention in parasitology (1,2). Dogs infected with canine VL (CVL) are an impor- for the indication of possible new targets in the diagnosis tant reservoir for VL (2) and by controlling canine VL, the and treatment of and vaccination against protozoan transmission cycle of VL to humans may be disrupted. parasites such as Leishmania (5,10). The available anti-leishmanial drugs have important The importance of proteome identification of protozoa side-effects and there is growing evidence of drug secretions has been highlighted (11,12). Studies have resistance in leishmaniasis (3,4). In the absence of suitable shown that the antigens from Leishmania parasites that drugs for VL, using proteomic techniques to identify new are able to stimulate Th1 cells are appropriate candidates markers for diagnosis, treatment and vaccination is an for designing vaccines against leishmaniasis (13,14). appropriate strategy for the control of leishmaniasis in Secretions of Leishmania promastigotes as activators of humans and animal reservoirs (5). the host immune response have been suggested to be

1548 Research article EMHJ – Vol. 26 No. 12 – 2020 suitable sources of antigens for the design of vaccines gel loading buffer (6X) consisting of 375 mM Tris-HCl and diagnostic tests in leishmaniasis (15,16). (pH 6.8), 12% SDS, 60% glycerol, 30% 2-mercaptoethanol Given these issues and the ability of proteomic and 0.6% bromophenol blue. Then, gels were run using an technology to provide information on secreted proteins electrophoresis system (Bio-Rad, United States of Ameri- from Leishmania parasites, our study aimed to identify ca). immunoreactive proteins in the secretions of L. infantum In the next step, the sample lanes were transferred promastigotes using sera of dogs infected with CVL. (Voltage 20, 1 h) from the gel to a polyvinylidene difluoride Identification of these proteins might open a new path for membrane (Bio-Rad, USA). After the transfer, 3% bovine the effective diagnosis and treatment of and vaccination serum albumin in phosphate buffered saline was used against CVL in the future. for blocking the non-specific binding sites on the polyvinylidene difluoride membrane (12 h at 4 °C). Pooled Methods sera from five CVL-infected dogs (asymptomatic and Obtaining secretions symptomatic) were used to probe the membranes (19). All CVL-infected and non-infected sera had been previously L. infantum (MCAN/IR/07/Moheb-gh strain: from CVL-in- checked for CVL using the direct agglutination test. fected dogs) promastigotes were mass cultivated at 25 °C Pooled sera from non-infected dogs were used as negative in Schneider insect culture medium (Sigma Chemical control. Antibody binding proceeding was done with Co., United States of America) supplemented with 20% 1:1000 dilutions of primary anti-sera in skim milk (2 h at (v/v) bovine serum (heat-inactivated at 56 °C for 50 min), room temperature). After three washes (15 min each) with 100 U/mL penicillin and 100 μg/mL streptomycin. The phosphate buffered saline containing 0.5% Tween-20, promastigotes were collected in the exponential growth the rabbit anti-dog IgG (1:4000 dilutions; Abcam, USA) phase (on the third day) by centrifugation at 2000 × g was then allowed to react (1.5 h at room temperature). for 10 min at 4 °C and then washed three times with se- Finally, the immunoreactive bands were detected using rum-free RPMI-1640 medium (Shelmax Co., China). diaminobenzidine tetrahydrochloride substrate (Sigma, 9 Washed promastigotes (6 × 10 promastigotes) Germany). The ChemiDoc MP Imaging System (Bio-Rad, were transferred to 10 mL serum-free RPMI-1640 to USA) was used to scan the bands obtained. To confirm the obtain secretions. After checking the viability of the results, the experiment was repeated three times using promastigotes at different times using flow cytometry sera from different CVL-infected and non-infected dogs. and propidium iodide, the secretions were collected after 72 h. The secretions obtained were centrifuged at Western blotting 9000 × g for 30 min at 4 °C and the supernatants were The protean isoelectric focusing cell system (Bio-Rad, collected (17). USA) was used for isoelectric focusing. About 200 μg of Deionization and lyophilization of secretions the protein sample was added for each immobilized pH gradient strip (pH 3–10 nonlinear, 18 cm) by active rehy- Contamination of the secretions with the ions (salts) dration (50 V, 20 °C, 14 h) in rehydration buffer (8 M urea, stops the isoelectric focusing stage. To remove these 2 M thiourea (Merck, Germany), 0.3% w/v dithiothreitol, ions, 50 mL of supernatant were aliquoted in dialyzed 2% w/v CHAPS, 2% vol/vol immobilized pH gradient buff- bags containing a ethylenediaminetetraacetic acid (ED- er (pH 3–10) and bromophenol blue) followed by isoelec- TA)-free protease inhibitor cocktail (Roche, Germany) at tric focusing for a total of 62 000 Vh. 1 × final concentration. The mixture was dialyzed over- night at 4 °C using a membrane (with a 14 kDa molecu- After isoelectric focusing, each strip was equilibrated lar mass cut-off) in 10 L of 1 mM ammonium bicarbonate in 10 mL equilibration buffer (6 M urea, 50 mM Tris, buffer (Sigma) with four solution changes (18). The dialyz- pH 8.8, 2% w/v SDS, 30% w/v glycerol) containing ed secretions were frozen and lyophilized to dryness. As 65 mM dithiothreitol (in the first step) and 135 mM a negative control, this procedure was repeated with the iodoacetamide (in the second step) at room temperature RPMI-1640 without promastigote secretions. Lyophilized for 15 min. Two-dimensional gel electrophoresis followed proteins were resuspended in lysis buffer (7 M urea, 2 M by Western blotting was done using the same procedures thiourea, 4% CHAPS and 2% immobilized pH gradient described earlier. To confirm the results, each experiment buffer (pH 3–10); GE Healthcare, Sweden), aliquoted and was repeated three times using pooled sera from different stored at –70 °C. The protein concentration was deter- CVL-infected and non-infected dogs. mined using Bradford assay and bovine serum albumin After the immunodetection step, GS‑800 calibrated (Sigma, Germany) as standard. densitometer (Bio‑Rad) and Prodigy SameSpots software (version 1.0) (Nonlinear Dynamics, United Kingdom of Gel electrophoresis and Western blotting Great Britain and Northern Ireland) were used to scan About 40 µg of the secreted proteins recovered were elec- the spots and analyse the digital images, respectively. The trophoresed using sodium dodecyl sulfate-polyacryla- reference image was an image with the greatest number mide gel electrophoresis (SDS-PAGE) on 4% stacking gels of spots. Each spot was analysed in a semi‑automated over 12% separating gels (Roche Applied Science, Germa- way and background intensity was subtracted from each ny). Sample lysates were boiled at 100 °C for 5 min in SDS image.

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Isolation of immunoreactive spots Figure 1 Western blotting of the secretions on the polyvinylidene difluoride membrane: a) ladder, b) probed After mapping the immunoreactive spots on the mem- membrane with sera of dogs infected with canine visceral brane, two-dimensional gel electrophoresis was conduct- leishmaniasis, c) probed membrane with sera of dogs ed again with the secreted proteins lysate. Coomassie without canine visceral leishmaniasis brilliant blue staining (containing 8% ammonium sulfate (Sigma, USA), 1.6% orthophosphoric acid (Sigma, USA), 20% methanol (Merck, Germany), and 0.12% Coomassie blue G 250 (Merck, Germany)) was used for visualization of spots (overnight incubation) (20). After staining, gels were destained with distilled water. Finally, the immuno- reactive spots identified on the membrane were punched from the gel using a pipette. In-gel digestion of protein samples and mass spectrometry In-gel digestion of protein samples and mass spectrom- etry analysis were done according to the protocol of the metabolomics and proteomics laboratory technology facility, Department of Biology, University of York, Unit- ed Kingdom (20). According to the company procedures, MASCOT scores of more than 62 are significant P( < 0.05). Western blotting and identification of immunoreactive proteins by mass spectrometry Database search We extracted and lysed secretions of L. infantum pro- The mass spectra generated by matrix-assisted laser de- mastigotes. Since the aim of our study was to identify sorption/ionization time-of-flight mass spectrometry immunoreactive proteins in the secretions of L. infantum (MALDI TOF/TOF MS) were searched against peptide promastigotes, we separated proteins in lysates by using masses in the UniProt database (555 594 sequences, isoelectric focusing over a pH range from 3 to 10 and then 199 016 217 residues) (Table 1) and also the NCBI database two-dimensional gel electrophoresis. Three gels were run (132 460 369 sequences; 48 620 496 129 residues) (Table 2). for each test. We detected more than 1000 spots and about Ethical considerations 100 immunoreactive spots on each of the gels and polyvi- Experiments with animals were done following guide- nylidene difluoride membranes, respectively. We isolated lines of the Institutional Animal Care and Committee on 13 repeatable and intense immunoreactive spots from the Ethics of Animal Experimentation of the Shiraz Universi- ty of Medical Sciences. Figure 2 Immunoproteome of the secretions on the Results polyvinylidene difluoride membrane: a) probed membrane with sera of dogs infected with canine visceral leishmaniasis, Viability of promastigotes b) probed membrane with sera of dogs without canine visceral leishmaniasis, c) selected spots of gel for mass When we obtained secretions, to decrease the release of spectrometry analysis secretory proteins from dead promastigotes to the secre- tions, we carried out propidium iodide staining to check the viability of L. infantum promastigotes. The propidium iodide results showed that the best time for collecting the secretions with a high concentration was 72 h after cul- tivating in serum-free RPMI-1640 medium. The rate of promastigotes viability at this time was 83% (17). SDS-PAGE and Western blotting Before doing the two-dimensional gel electrophoresis fol- lowing Western blotting, we determined the molecular weights of the immunoreactive protein bands in the se- cretions. As shown in Figure 1, we detected several sharp bands between 25 and 35 kDa and 66.2 and 116 kDa. We also saw a weak band between 45 and 66.2 kDa. Perform- ing Western blotting before 2-DE-Western blotting facil- itates the identification of immunoreactive spots on the polyvinylidene difluoride membrane and gel.

1550 Research article EMHJ – Vol. 26 No. 12 – 2020 gel for mass spectrometry analysis (Figure 2). Of these potential action of chitin-binding proteins in Leishmania spots, nine immunoreactive proteins were characterized and gene sequencing and cloning of chitin-binding by MALDI TOF/TOF MS. Due to contamination with ker- proteins (23) might be useful to understand the role of atin, three spots showed spectra dominated with kera- chitin-binding proteins in the biology of Leishmania tin. The identified proteins were chitin-binding protein, parasites. immune inhibitor A (immune In A), a peptide matched The function of immune In A in Leishmania parasites is to bacillolysin (δ-endotoxin), a single peptide match to still not known; however, this protein has been described hs1vu complex proteolytic subunit-like, a single peptide as a neutral metalloprotease in bacteria (25). Based on the match to chain A crystal structure of selenomethionine, presence of metalloproteases in Leishmania parasites and iron superoxide dismutase, phospholipase C, and some their involvement in parasite virulence, the discovery of proteins matched to enterotoxins. immune In A as a possible metalloprotease in Leishmania We used the L. infantum genome project database parasites suggests that this protein may be of clinical (www.genedb.org) and published literature for the interest for leishmaniasis prognosis and the prediction identification of multiple functions of the detected of treatment efficacy (26). Since IgA protease is the only proteins. The scores of all the proteins obtained were homologous protein of immune In A, the detection of significant (> 62). According to the mass spectrometry anti-immune In A in CVL- and VL-infected sera might data, spot number 17 (SEC 13) was identified as “immune suggest new approaches using tools based on immune In A” and “selenomethionine” in the Uniprot and NCBI In A for the diagnosis of leishmaniasis in the future (27). databases, respectively. We identified a peptide that matched bacillolysin (δ-endotoxin). Bacillolysin is a virulence factor and Discussion lethal toxin in bacteria (28). Interestingly, the role of the We applied an immunoproteomic approach on secretions disulfide bond A as a homologue of the protein disulfide of L. infantum promastigotes, using pooled sera from isomerase is associated with the production of toxins in CVL-infected dogs (asymptomatic and symptomatic), to bacteria (29). Because protein disulfide isomerases are find immunoreactive proteins that could be possible new important proteins in the pathogenicity of Leishmania targets for diagnosis and treatment of, and vaccination parasites, the possible expression of such endotoxins against CVL. The use of pooled sera might reduce the ef- in these parasites could be related to protein disulfide fect of individual animal immune response variations on isomerases (29,30). Due to the scarce data on endotoxins L. infantum antigens. in Leishmania parasites, molecular techniques including Chitin-binding protein as an immunoreactive gene expression and quantitative real-time polymerase protein in the secretions of L. infantum promastigotes chain reaction could be used to confirm the production has been previously reported in Toxoplasma gondii (21). of endotoxins in these parasites. Chitin-binding protein is part of chitinase enzyme and The survival, virulence and proteolytic functions synergistic effects of chitin-binding proteins on chitinases of hs1vu in Leishmania parasites have been described in have been described in bacteria (22). Although the activity previous studies (31–33). In addition, the relationship of chitinase is two-to-four- fold higher in amastigotes between hs1vu and 3M3I protein (a hypothetical protein than in promastigotes in vitro (23), in a previous study in L. major likely involved in nucleotide metabolism) may on the secretions of L. donovani, chitinase and chitin- be helpful to elucidate the metabolic function of hs1vu binding proteins were not detected in mass spectrometry in Leishmania parasites (34). The potential and critical results (24). More investigations on the elucidation of the functions of hs1vu, and the overexpression of this protein

Table 1 Identification of immunoreactive proteins in the secretions ofLeishmania infantum promastigotes (UniProt) Spot name No. of Protein name No. of Mr pI (theoretical) Score Protein Accession spots on matched (theoretical) sequence no. gel peptides coverage (%) SEC 5 10 PLC 4 32.3 7.14 101 7 P09598 SEC 6 6 A single 1 47.8 4.23 90 35 P80567 peptide match to Enterotoxin (fragment) SEC 9 8 PLC 2 32.3 7.14 101 7 P09598 SEC 12 9 PLC 4 32.3 7.14 275 14 P09598 SEC 13 17 A single 1 74.9 5.13 54 1 P23382 peptide match to Immune In A Mr = molecular weight; pI = isoelectric point; PLC = phospholipase C.

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Table 2 Identification of immunoreactive proteins in the secretions ofLeishmania infantum promastigotes (NCBI) Spot No. of spots Protein name No. of matched Mr pI (theoretical) Score Protein Accession no. name on gel peptides (theoretical) sequence coverage (%) SEC 1 4 A single peptide 1 24.2 6.07 73 5 XP_001469616.1 match to hs1vu

SEC 2 7 A single peptide 1 83.3 5.75 73 1 4YU5_A match to chain A, crystal structure of selenomethionine SEC 4 14 Chitin-binding 3 49.9 6.18 295 9 WP_001035088.1 protein SEC 6 6 Enterotoxin 40 kDa 2 43.09 6.85 171 6 CRG01534.1 subunit SEC 8 2 A single peptide 1 36.3 6.01 85 4 EOP01994.1 match to antigen SEC 10 12 A single peptide 1 62.6 5.78 77 2 EEM05310.1 match to bacillolysin (insecticidal δ-endotoxin) SEC 11 1 Iron superoxide 2 26.5 8.46 185 12 XP_001463371.1 dismutase SEC 12 9 Phospholipase C 3 32.2 6.5 212 11 WP_002010569.1 SEC 13 17 A single peptide 1 83.3 5.75 82 1 4YU5_A match to chain A, crystal structure of selenomethionine

Mr = molecular weight; pI = isoelectric point. in the viscerotropic form of L. tropica (31) suggest a role anchor through phospholipase C and the induction of this protein as a valuable marker in the treatment and of GP63-shedding via phospholipase C in Leishmania diagnosis of CVL and VL in a clinical setting. parasites are related to the virulence and pathogenicity Selenoproteins are involved in the regulation of functions of phospholipase C in these parasites (43– oxidative stress in the cells. Isolation of leishmanial- 45). Nevertheless, the exact role of phospholipase C selenomethionine derivatives from L. donovani proteins, is unknown in Leishmania parasites so far. Given the and the sequencing of the gene encoding this protein in aforementioned functions of phospholipase C in the Kinetoplastida support our detection of selenomethionine pathogenicity of Leishmania parasites and also the role through mass spectrometry assays (35,36). of phospholipase C in hydrolysis of miltefosine, the use of phospholipase C-inhibitors can be evaluated as a Leishmania We also identified Fe-SOD which protects therapeutic target in CVL and VL in the future (46). parasites against radical superoxide anions. The expression of SODs as conserved molecules with a Conclusion high degree of homology in Leishmania species (24,37,38) The isolation of high protein concentrations in proteom- highlights the possible use of these proteins in the ic studies on secretions provides reliable data. Since se- development of candidate drug and vaccine targets in creted antigens of Leishmania promastigotes are potential leishmaniasis. In recent years, nanovaccines against stimulants of the host immune system, the identified leishmaniasis have been evaluated by producing the immunoreactive proteins in our study might be valuable recombinant form of leishmanial-SODB1 and loading on proteins for developing diagnostic candidates and vac- the chitosan nanoparticles (39). cine targets in the future. In addition, according to the The report of phospholipase C-orthologue genes main roles of such molecules in metabolism pathways, and phospholipase C-related signalling pathways in survival and pathogenicity of Leishmania parasites, they protozoa in previous studies confirms our results on the could be possible therapeutic targets for CVL in the fu- expression of phospholipase C in secretions of Leishmania ture. Validation of our results – the proteins we found parasites (40,41). It has been suggested that the escape of expressed in Leishmania parasites – through further protozoan parasites from parasitophorous vacuoles could laboratory techniques including gene cloning, Western be mediated by phospholipase C (42). The expression blotting, enzyme-linked immunosorbent assay (ELISA) of inositol phosphosphingolipid phospholipase C-like and quantitative real-time polymerase chain reaction is protein, the cleavage of the glycophosphatidyl-inositol warranted.

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Funding: National Institute for Medical Research Devel- number 971405). opment (NIMAD), Tehran, Islamic Republic of Iran (grant Competing interests: None declared.

Identification de protéines immunoréactives dans les sécrétions des promastigotes de Leishmania infantum : une approche immunoprotéomique Résumé Contexte : Dans la Région méditerranéenne, Leishmania infantum est la principale cause de leishmaniose viscérale. Les chiens atteints de leishmaniose viscérale canine constituent un important réservoir de leishmaniose viscérale. La lutte contre la leishmaniose viscérale canine pourrait empêcher la transmission de cette maladie à l’homme. Les antigènes sécrétés par les promastigotes de Leishmania sont des stimuli potentiels du système immunitaire de l’hôte. Les techniques protéomiques facilitent l’identification de nouveaux marqueurs protéiques. Objectifs : La présente étude visait à identifier des protéines immunoréactives dans les sécrétions de promastigotes L. infantum qui pourraient être utilisées pour le diagnostic et le traitement de la leishmaniose viscérale canine et la mise au point de vaccins contre cette maladie. Méthodes : Les sécrétions de promastigotes L. infantum ont été obtenues à partir de la culture de 6 × 109 promastigotes dans un milieu sans sérum RPMI-1640 pendant une période de 72 h. Après déionisation et lyophilisation, on a utilisé une électrophorèse bidimensionnelle en gel pour séparer les protéines, suivie d’un transfert de type Western. Treize points immunoréactifs communs et répétables ont été analysés par spectrométrie de masse. Résultats : Neuf protéines ont été identifiées par spectrométrie. La plupart de ces protéines étaient impliquées dans les voies métaboliques, la survie et la pathogénicité des parasites Leishmania. La phospholipase C, l’inhibiteur immunitaire A, la protéine de liaison à la chitine et un peptide unique correspondant à la structure cristalline de la chaîne A de la sélénométhionine ont été observés dans les sécrétions de promastigotes de L. infantum. Conclusions : Les protéines identifiées dans les voies métaboliques, la survie et la pathogénicité des parasites Leishmania sont des cibles possibles qui pourraient être utilisées pour le diagnostic et le traitement de la leishmaniose viscérale canine et la mise au point de vaccins contre la maladie à l’avenir.

" " حتديد الربوتينات املناعية التفاعلية يف إفرازات ُم َش ِّي َقة الليشامنيا الطفلية : هنج الربوتيوميات املناعية ساجد رشيدي، بول نجويوا، زهرة جمتهدي، هبادور شهرياري، كوروش كاالنتار، غالم رضا حاتم اخلالصة يفاخللفية: إقليم رشق املتوسط، ُتعترب "الليشامنيا الطفلية "السبب الرئييس لداء الليشامنيات احلشوي. ُويعترب الكالب املصابون بداء الليشامنيات احلشوي ً مستودعا ًمهام له. ويمكن أن ّي تؤدمكافحة داء الليشامنيات احلشوي يف الكالب إىل وقف انتقاله إىل البرش. وقد تكون مستضدات ُم َش ِّي َقة "الليشامنيا " ُاملفرزة هي حمفزات حمتملة للنظام املناعي يف جسم املضيف. ومن شأن تقنيات الربوتيوميات أن ُتسهل من إمكانية حتديد الواسامت الربوتينية اجلديدة. " " هدفتاألهداف: هذه الدراسة إىل حتديد الربوتينات املناعية التفاعلية يف إفرازات ُم َش ِّي َقة الليشامنيا الطفلية ، والتي من املمكن أن تكون مستهدفات حمتملة لتشخيص وعالج داء الليشامنيات احلشوي يف الكالب وتطوير لقاح مضاد هلذا املرض. RPMI " " طرق البحث: ُحصل عىل إفرازات ُم َش ِّي َقة الليشامنيا الطفلية من مزرعة ُم َش ِّي َقة 6×910 يف وسط 1640- خال من األمصال خالل فرتة 72 ً.ساعة وبعد إزالة التأيني والتجفيد بالتجميد، ُخدم استاثنان من أجهزة الرحالن الكهريب اهلالمي ثنائي األبعاد لفصل الربوتينات، َوأعقب ذلك إجراء لطخة ويسرتن. ُخدم واستقياس طيف الكتلة يف حتليل ثالثة عرش ًموضعا ًمناعيا ًتفاعليا ًمشرتكا ًومتكررا. النتائج: حدد قياس طيف الكتلة تسعة بروتينات. وكان أغلبها ً يفموجودا مسارات التمثيل الغذائي، والبقاء عىل قيد احلياة، وإمراضية طفيليات A C " " " " الليشامنيا . وقد لوحظ يف إفرازات ُم َش ِّي َقة الليشامنيا الطفلية وجود فوسفوليباز ، واملثبط املناعي ، والربوتني الذي يربط الكيتني، ومطابقة A ْالببتيد الواحد لسلسلة الرتكيب البلوري للسيلينوميثيونني . االستنتاجات: ُتعترب الربوتينات ُاملحددة يف مسارات التمثيل الغذائي، والبقاء عىل قيد احلياة، وإمراضية طفيليات "الليشامنيا" ُمستهدفات حمتملة يمكن استخدامها يف تشخيص داء الليشامنيات احلشوي يف الكالب ومعاجلته وتطوير لقاحات مضادة هلذا املرض يف املستقبل.

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National food policies in the Islamic Republic of Iran aimed at control and prevention of noncommunicable diseases

Masoumeh Moslemi,1 Mehrnaz Kheirandish,2 Ramin Nezhad Fard Mazaheri,3,4 Hedayat Hosseini,5 Behrooz Jannat,1 Vahid Mofid,5 Atefeh Moghadd- am 6 and Nader Karimian 6

1Halal Research Centre, Iran Food and Drug Administration, Tehran, Islamic Republic of Iran. 2Department of Assessment and Control of Prescribing and Use of Medicines and Health Products, Iran Food and Drug Administration, Tehran, Islamic Republic of Iran. 3Division of Food Microbiology, Department of Pathobiology, School of Public Health, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran. 4Food Microbiology Research Centre, School of Public Health, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran. 5Department of Food Science and Technology, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Sciences and Food Technology, Shahid Beheshti Univer- sity of Medical Sciences, Tehran, Islamic Republic of Iran. 6Department of Foods and Beverages, Iran Food and Drug Administration, Tehran, Islamic Republic of Iran. (Correspondence to: Mehrnaz Kheirandish: [email protected]).

Abstract Background: Diet plays an important role in the risk of noncommunicable diseases. In the Islamic Republic of Iran, national activities were started after release of the World Health Organization’s (WHO) action plan on prevention and control of noncommunicable diseases. Aims: This study describes national food policies implemented by the government in order to reduce noncommunicable diseases in the country in line with WHO action plan. Methods: Newly adopted food standards and regulations linked to noncommunicable diseases from 2013 to 2018 were reviewed and the maximum permitted levels of salt and trans and saturated fats were compared in the old and new stand- ards. Nutritional traffic light labelling to raise public awareness of healthy diets was evaluated. Results: Fifteen food standards associated with eight food items that make up a large share of the daily Iranian food basket and three that make up a small share were evaluated. Policies on salt included reduction in maximum permitted percentage in bread, cheese and doogh (a fermented drink) to 1%, 3% and 0.8%, respectively. For trans and saturated fats, maximum permitted percentages were set as 2–5% and 30–65% of edible oils and fats, respectively. Nutritional traffic light labelling, which indicates the content of salt, sugar, fat and trans fat in foods, has been mandatory for all foods since 2016. Conclusions: In view of the polices implemented to reduce the salt and fat/oil content of foods, significant decreases in noncommunicable diseases are expected in coming years in the country. However, further studies are needed to show the effectiveness of the interventions. Keywords: diet, nutrition policy, noncommunicable diseases, Iran Citation: Moslemi M; Kheirandish M; Mazaheri R; Hosseini H; Jannat B; Mofid V; et al. National food policies in the Islamic Republic of Iran aimed at prevention of noncommunicable diseases. East Mediterr Health J. 2020;26(12):1556–1564. https://doi.org/10.26719/emhj.20.024 Received: 03/03/19; accepted: 02/09/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction and socioeconomic characteristics (4,5). Therefore, one of the main global challenges in designing strategies Noncommunicable diseases (NCDs) are chronic disor- to control and manage NCDs in large countries such ders caused by non-infectious agents. NCDs kill 41 mil- as the Islamic Republic of Iran is modification of food lion people annually, which represents 71% of all deaths traditions. Practical recommendations to follow a healthy worldwide (1). Based on World Health Organization lifestyle are regularly published by WHO. In 2013, WHO (WHO) reports, annual deaths from NCDs are mostly made a global call for a 25% decrease in premature deaths linked to cardiovascular diseases (44%), cancers (22%), res- from NCDs in people aged 30–70 years by 2025 (6). piratory diseases (10%) and diabetes (4%) (1). NCDs are an Furthermore, Member States of WHO endorsed the 2013– important health concern in the Islamic Republic of Iran; 2020 action plan that focuses on four behavioural risk the annual death rate from NCDs represents about 82% factors for NCDs: unhealthy diet, harmful use of alcohol, of the total mortality in the country (2). National studies insufficient physical activity and tobacco use. The action show a 14.5% increase in deaths from NCDs in the past 20 plan describes 25 indicators classified under nine targets years (3). This is of concern, especially as the population (3,6) to help countries develop their national strategies for is ageing. decreasing NCDs. To respond to this call and the action Several factors should be considered when developing plan, The Ministry of Health and Medical Education of and implementing strategies to reduce NCDs. For example, Iran established the national NCD committee in 2015 diet, and preparation and consumption of foods vary in with the aim of integrating all decisions and activities on different societies and according to demographic, cultural the prevention and control of NCDs at the national level

1556 Research article EMHJ – Vol. 26 No. 12 – 2020 in line with the WHO global call. Because NCD mortality Organization. Furthermore, the maximum permitted lev- from other causes not included in WHO nine targets is els of salt, and trans and saturated fats in old and revised high in the country, four further targets were added to standards were compared. The activities of the Iran Food the list by the health ministry. These targets were: zero and Drug Administration to raise public awareness about trans fatty acids in all manufactured food products, healthy food consumption were also assessed. reduced traffic injuries, reduced drug abuse and access to Since one of the nine NCD targets introduced by treatment for mental diseases. WHO is salt reduction and several national policies Similar to other countries, dietary risk factors are have been put in place to decrease and control daily salt significant contributors to NCDs in the Islamic Republic consumption, the population attributable risk of the of Iran, and their assessment and management are percentage of the incidence of disease that is due to salt fundamental to preventing NCDs (3,7,8). Thus, close was calculated using the following equation: collaboration between the public sector, private health Population attributable risk % = Pe × (RR – 1)/ associations and the food industry is needed to establish [P × (RR – 1) + 1] healthy food policies to achieve national and international e where, P is the proportion of the population exposed to targets. In the Islamic Republic of Iran, the Food and Drug e Administration is responsible for national food safety the risk factor (salt in this case) and RR is the relative risk and, as a member of the national NCD committee, works of the risk factor (salt). closely with other key players in food and nutrition fields Results to improve the effectiveness of food policies and strategies linked to NCDs. Many interventions and factors have Several interventions such as modifications of existing important roles in the prevention of NCDs, including standards or adoption of new standards have been imple- food reformulation, labelling, monitoring, and public mented in the country based on the international recom- awareness and marketing (7). For example, socioeconomic mendations of daily intakes of: < 5 g of salt, < 10% total factors, such as incentives to choose larger packages energy intake from saturated fatty acids and < 1% total through advertisements and price encouragements, energy intake from trans-fats (10). We identified eight may negatively affect dietary patterns (9). To minimize food items that make up a large share of the daily Irani- the adverse effects of diet on the prevalence of NCDs an food basket and three that make up a small share. As in the Islamic Republic of Iran, international guidelines shown in Table 1, 17 standards were identified for these and recommendations on food intake were studied by food products, 15 of which were selected for further as- stakeholders including regulatory experts such as risk sessments after removing duplications. managers and academic staff. As a result, the maximum permitted levels of salt and saturated and trans fatty acids Interventions on salt in food in the national regulations were modified based Since 2015, the Iran Food and Drug Administration has on Iranian dietary patterns. These modifications were taken action on bread, doogh (Iranian fermented drink) used for staple foods such as bread, dairy products and and cheese as the major sources of salt intake in the oil products. In parallel, to increase consumer awareness country. No new standards have been developed for these and its contribution to preventive mechanisms, a new food items. As shown in Table 2, three standards were graphical feature was designed and used on all food revised with regard to the permitted level of salt in each packaging – a nutritional traffic light. food item. The permitted percentage of salt in bread was In this study, policies and interventions adopted in gradually reduced from 1.8% to 1.0% to adapt consumer the Islamic Republic of Iran to decrease NCDs following taste, a decrease of 44%. With regard to foods that make the WHO action plan were reviewed. As the Islamic up a small share of the daily food basket, a new nation- Republic of Iran is a pioneer in the region in adopting al standard was established and implemented in 2015 on measures to reduce NCDs, especially for trans fatty acids the amount of edible salt in food products such as canned and nutritional traffic lights, we aimed to share our foods, tomato pastes, processed olives, sauces and pick- experiences in NCD control with other countries in the les (16). In addition, salt use was banned in probiotic yo- region. ghurts in 2018 (15). Based on epidemiological data, the relative risks of Methods cardiovascular diseases and stroke associated with salt are In this study, a comprehensive review was carried out 1.14 and 1.23, respectively (26). The population attributable on newly adopted food standards and regulations by the risk of both diseases in the Islamic Republic of Iran Iran Food and Drug Administration and the Iran Nation- before the modified salt standards were implemented al Standards Organization which addressed the WHO was calculated. For the analysis, Pe = 97.66% was used target of a 25% decrease in premature deaths from NCDs based on a previous study (27). Therefore, population by 2025. First, food products associated to NCD policies attributable risk % was 12.03% for cardiovascular disease were identified. Then, all relevant standards and regu- and 18.34% for stroke before the modified standards. lations, including newly adopted or modified versions, were extracted from the official websites of the Iran Food Interventions on oils and Drug Administration and Iranian National Standards To follow WHO recommendations, a number of restric-

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Table 1 Number of standards on salt, and trans and saturated fats related to food items that make up large and small shares of the daily Iranian food basket Component Food product New Modified standard standard Salt Large share (Ref.) Small share (Ref.) Bread (11,12) – 2 Fresh cheesea (13) – 1 Doogh (Iranian fermented drink) (14) – 1 Probiotic yoghurt (15) – 1 Other productsb (16) 1 – Oil Trans/saturated fat Frying oil (household & industry use) – 1 (17) Semisolid oil for household use (18) – 1 Table margarine and spread – 1 margarine (19) Minarine & sweetened minarinec (20) – 1 Shortening (21) – 1 Palm oil Cheese (fresh cheesea, lactic cheese, – 3 pre-cheese) (13,22,23) Butter (pasteurized butter, spread – 2 butter) (24,25) Minarinec (20) – 1

Ref. = reference. aSimilar standards have been developed for both indices. bExamples are canned foods, tomato paste, processed olives, sauces and pickles. cSimilar standards have been developed for both indices. tions have been imposed on oil products in the Islamic Re- been banned since 2015. public of Iran since 2015. The trans fat level was reduced to 2% and saturated fat level to 30% in final oil products Nutritional traffic light for household use. For frying oils added to food products A nutritional traffic light system has been designed us- in industry and minarine (a cream-like product used in ing three colours – green, orange and red – to indicate confectionary), higher saturated fat levels were allowed low, medium and high levels of ingredients, respectively compared with household products (Table 3). Moreover, (Table 4). Calculation of amounts and assigning the col- higher maximum permitted levels of trans and saturated ours for each food was based on the quantities per 100 g fats were set for shortening because it is directly used in of solid foods, 100 mL of liquid foods or the serving size. oil industries and makes a negligible contribution to dai- If the serving size is less than 100 g or 150 mL, the levels ly food baskets (Table 3). under heading of per 100 g/100 mL are used. Otherwise, Annual palm oil imports were restricted in the the levels in the last column (per serving size) must be country in 2014, leading to a drop in imports from 750 000 used. Then, if the product does not match with the last tons in 2013 to about 465 000 tons in 2017 (unpublished column, the colour is selected by converting the quantity report). Furthermore, import tariffs on palm oil increased per 100 g or 100 mL and using numbers of other columns substantially from 2–4% in 2013 to 26–40% in 2016 (28). As shown in Figure 1, the amounts of a parameter are (unpublished report). Production of analogue foods using calculated and inserted in the food label. vegetable oils such as analogue cheese and butter, and Since early 2016, nutritional traffic light labelling addition of palm kernel oil/palm stearin to minarine have on food packages is mandatory for all imported and

Table 2 Changes in maximum permitted percentage of salt in foods that make up a large share of foods bought and consumed Food (reference) Before (%) After (%) Decrease (%) Base year Bread (11,12) 1.8 1.0 44 2016–2017 Cheese (13) 4.0 3.0 25 2015 Doogh (Iranian fermented drink) (14) 1.0 0.8 20 2015

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Table 3 Changes in permitted percentage of trans and saturated fats in oil products Product (Ref.) Trans fat (%) Saturated fat (%) Before 2015 After 2015 Before 2015 After 2015 Household use Frying oil (17) 2 2 No limits 30 Semisolid oil (18) 5 2 30 30a Table margarine (19) 10 2 40 48 Spread margarine (19) 5 2 30 35 Minarine (20) 5 2 No limits 60 Industry use Frying oil (17) 2 2 No limits 45 Minarine (20) 5 2 No limits 60 Shortening (21) 10 5 No limits 65

Ref. = reference. aThis further decreased to 25% in 2018. domestic foods, except for products that are not authorities brought in new restrictions. Mandatory re- chemically processed or formulated, such as vegetables, formulation of popular foods is the most cost-effective spices, vinegar, lemon juice, tea, infusions, coffee, honey, approach to decreasing disease burdens associated to salt dates, flour and barberry. (33–35). Therefore, we examined salt content of and regu- lations on staple foods such as bread, cheese and doogh. Discussion The Iran national survey on average daily Unhealthy diet is one of the four behavioural risk factors consumption of food reported a daily consumption of associated with NCDs (6). As people of all ages are more 310 g of bread, 16 g of cheese and 6 g of doogh per capita likely to be exposed to this risk factor than the other three (36). Based on these data, it is estimated that 2.65 g/ (tobacco use, harmful use of alcohol and physical inactiv- day of salt has been removed from the food of every ity), food interventions to reduce the intake of certain Iranian after the adoption of new interventions in 2017. products to safer levels have been instigated by countries. Therefore, the current salt intake is estimated to be 6.87 g/day. We also showed that 12% of cardiovascular Salt evidence diseases and 18% of strokes could be attributed to high Salt is necessary for normal body function and food pres- salt intake in 2016 (before the regulations). Therefore, ervation. Nonetheless, excessive daily salt intake results large decreases in these diseases are expected in coming in diseases such as high blood pressure, cardiovascular years as a result of the reduction in salt intake through diseases and gastric cancers (29,30). For example, sodium staple foods. It is worth noting that the daily salt intake is intake of 3480 mg/day, equal to 8.8 g/day of salt, was the still higher than that recommended by WHO and further main contributor to cardiometabolic diseases, mainly in restrictions through reformulations are not practical elderly people, in the United States of America (31). This because of technical limitations. For example, other than intake is similar to the daily intake of salt in the Islamic the flavour and preservative roles of salt, addition of salt Republic of Iran in 2016 – 9.52 g (27). Based on the clinical to dough for bread baking is responsible for texture due adverse effects, WHO has recommended a maximum salt to the electrostatic interactions between amino acids and intake of 5 g/day, which allows normal function of the hu- effects on hydration of proteins (37). Therefore, to achieve man body with no adverse effects on health (32). Since the further reduction in salt intake, consumers’ awareness of national salt intake in the Islamic Republic of Iran was their salt consumption should be promoted. About 50– about twice the WHO recommended level, regulatory 60% of daily salt intake is from salt that is directly added

Table 4 Cut-off points for the nutritional traffic light labelling (28) Index Low level Medium level High level Per 100 g Per Per 100 g Per 100 mL Per 100 g Per Per serving size 100 mL 100 mL Salt ≤ 0.3 ≤ 0.3 > 0.3 to ≤ 1.5 > 0.3 to ≤ 0.75 > 1.5 > 0.75 > 1.8 > 0.9 Sugar ≤ 5 ≤ 2.5 > 5 to ≤ 22.5 > 2.5 to ≤ 11.25 > 22.5 > 11.25 > 27 > 13.5 Fat ≤ 3 ≤ 1.5 > 3 to ≤ 17.5 > 1.5 to ≤ 8.75 > 17.5 > 8.75 > 21 > 10.5 Trans fatty acid ≤ 0.5 ≤ 0.5 > 0.5 to ≤ 2 > 0.5 to ≤ 2 > 2 > 2 > 2 > 2

100 g is used for solid foods and 100 mL for liquid foods.

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Figure 1 Nutritional traffic light label used for food products known carcinogenicity of monochloropropane diol in the Islamic Republic of Iran esters which is mainly formed in palm oil during the refining processes(47) , were important health concerns. Therefore, the Iran Food and Drug Administration aimed to decrease saturation levels of fats by requiring industries to use other vegetable oils. The main strategy was setting a maximum permitted saturation in popular household frying oils which previously was not limited, and similar policies were adopted for industrial frying oils. As a result, addition of palm oil to foods was restricted in national food industries and people’s exposures to the hazardous compounds decreased to safe levels. Today, Iranian oil industries use various oil fractions to produce food products under the modified regulations. For example, they use emulsifiers in the mixture of unsaturated vegetable oils with small portions of fully hydrogenated oils to prepare healthier semisolid to food by the consumer (38), which is currently equal to formulations compared with partially hydrogenated oils. 3.44–4.12 g/day in the Islamic Republic of Iran. These mixtures consist of about 70% common vegetable oils such as canola and sunflower, up to 25% of palm olein Oil evidence and a maximum 5% of fully hydrogenated oils. Therefore, WHO recommends that less than 1% and 10% of total di- recent formulations contain higher unsaturation rates etary energy intake per day should come from trans and and reduced levels of trans and saturated fatty acids saturated fats, respectively (39). Cardiovascular diseases compared with earlier formulations. impose heavy financial burdens on governments annual- Nutritional traffic light ly because of productivity losses and health care expens- es (40). Other than salt contribution, the high cardiovas- According to the Codex Alimentarius, “labeling includes cular disease rates are possibly due to the consumption any written, printed or graphic matter that is present on of saturated and trans fats (41,42). Trans fats have further the label, accompanies the food or is displayed near the hazards as they can induce thrombogenesis and ather- food including that for the purpose of promoting its sale ogenesis (41,42). Despite previous reports, new findings or disposal” (48). To minimize the negative contribution have shown that ruminant-produced and industrial trans of overweight and obesity to NCDs, simple policies to in- fatty acids adversely change the ratio of low-density lipo- form consumers, including nutritional labelling, were in- protein cholesterol to high-density lipoprotein cholester- troduced for preventive purposes in the Islamic Republic ol in the human body (43). However, the adverse effects of of Iran. Nutritional labelling helps consumers to choose industrial fatty acids are greater than those of ruminant healthy products within various commercial brands isomers in normal diets. This effect possibly occurs be- based on their daily food baskets and calorie intakes. This cause of the presence of bioactive components and nu- strategy also helps the government to control NCDs and trients in ruminant-derived foods containing trans fats reduce budgets for medical care as a result of NCDs. Ex- (43). Therefore, lower intake of these two fatty acids or periences in other countries show that nutritional traffic their substitution with cis unsaturated fatty acids results light labelling is a preferred method compared with other in healthier blood lipid profiles (43). Moreover, iso-caloric labelling guides such as octagons, nutritional claims, log- substitution of saturated fatty acids with cis unsaturat- os and numerical levels per serving sizes (49). Therefore, ed fatty acids, particularly polyunsaturated fatty acids, design of graphical feature showing total calorie, salt, results in lower rates of cardiovascular diseases and sig- sugar, fat and trans-fat indices was motivated by Iran nificant decreases in low-density lipoprotein and total FDA. Despite similar targets of nutritional labelling by cholesterol (40,44). Studies have also shown the negative different countries (50), differences exist in the details in role of saturated fatty acids in type 2 diabetes as saturated the labels. For example, most countries include the total fatty acids from milk and liquid oils increased the overall calorie, fat, sugar and salt in foods (50); however, level of risk of type 2 diabetes (45). trans fat was also added to the nutritional traffic light by Previously, the main source of trans isomers for the Iran Food and Drug Administration because of the humans included partially hydrogenated oils (46). clear involvement of trans fatty acids in cardiovascular However, the use of these oils has decreased because of diseases in the country. the evidence of their clinical adverse effects (41,42). In Studies that assessed the effectiveness of nutritional the Islamic Republic of Iran, similar to other countries, traffic light labelling on food selection have shown that restrictions on the production of partially hydrogenated raising consumer awareness and knowledge would oils have led to further use of palm oil because of its increase the effects of such interventions (51,52). Thus, cost–effectiveness. However, high levels of saturated the Iran Food and Drug Administration ran a health fatty acids, such as palmitic acid in palm oil and the campaign to introduce the nutritional traffic light

1560 Research article EMHJ – Vol. 26 No. 12 – 2020 labelling to people. The campaign included educational that, in addition to revising food product regulations and programmes at schools, interviews in the media and encouraging the food industry to reformulate food prod- public advertisements. However, this is the beginning of ucts, behavioural modifications should be considered nutritional traffic light labelling in the country and further by consumers to reduce their risk of NCDs as a result of research must be carried out on consumer perceptions their diet. In the Islamic Republic of Iran, salt levels in various foods, as well as saturated and trans fatty acids to have a better understanding of effectiveness of this in oil products, decreased through implementation of policy. new national strategies. Furthermore, nutritional traffic Conclusion light labelling was established as a strategy to raise public awareness. Further studies are needed to assess the effec- The Islamic Republic of Iran is a large country with a va- tiveness of these interventions in reducing NCDs in the riety of cultures and dietary behaviours. Our study shows Islamic Republic of Iran.

Acknowledgement We thank Dr. Heshmatollah Razavi Mousavi, Mr. Hooman Mohammad Raoufi, Mrs Zohreh Pourahmadi (from Iran Food and Drug Administration) and staff of the Iran National Standards Organization for their contribution in preparation of the adopted policies. Funding: None. Competing interests: Dr. Mehrnaz Kheirandish was Director General for Department of Assessment and Control of Prescribing and Use of Medicines and Health Products at Iran FDA from 2016 to 2020. Dr. Masoumeh Moslemi and Dr. Atefeh Fooladi Moghaddam worked at Iran FDA and Mr. Nader Karimian Khosroshahi currently works at Iran FDA. Dr. Hedayat Hosseini, Dr. Behrooz Jannat and Dr. Vahid Mofid were Director General for Department of Foods and Beverages at Iran FDA from 2012 to 2015, 2016 to 2017 and 2018 to 2019, respectively.”

Les politiques alimentaires nationales de la République islamique d’Iran visant la prévention et la maîtrise des maladies non transmissibles. Résumé Contexte : Le régime alimentaire joue un rôle important dans le risque de contracter des maladies non transmissibles. Après la publication du plan d’action de l’Organisation mondiale de la Santé (OMS) sur la prévention et la maîtrise des maladies non transmissibles, des activités nationales ont été mises en route en République islamique d’Iran. Objectifs : La présente étude décrit les politiques alimentaires nationales mises en œuvre par le gouvernement afin de lutter contre les maladies non transmissibles dans le pays conformément au plan d’action de l’OMS. Méthodes : Les normes et réglementations alimentaires récemment adoptées, liées aux maladies non transmissibles de 2013 à 2018, ont été examinées et les teneurs maximales autorisées en sel et en graisses saturées et en acides gras trans ont été comparées dans les anciennes et les nouvelles normes. Le système de feux tricolores pour l’étiquetage nutritionnel visant à sensibiliser le public aux régimes alimentaires sains a été évalué. Résultats : Quinze normes alimentaires associées à huit produits alimentaires qui constituent une grande partie du panier alimentaire quotidien iranien et trois qui en constituent une petite partie ont été évaluées. Les politiques relatives au sel comprennent la réduction du pourcentage maximum autorisé dans le pain, le fromage et le doogh (une boisson fermentée) à 1 %, 3 % et 0,8 %, respectivement. En ce qui concerne les graisses saturées et les acides gras trans, les pourcentages maximums autorisés des huiles et graisses comestibles ont été fixés respectivement à 2-5 % et 30- 65 %. L'étiquetage nutritionnel aux feux tricolores, qui indique les teneurs en sel, sucre, graisses et acides gras trans des aliments, est obligatoire pour tous les aliments depuis 2016. Conclusions : Les politiques mises en œuvre pour réduire la teneur en sel et en graisses/huiles des aliments devraient entraîner une baisse significative des maladies non transmissibles dans les années à venir dans le pays. Cependant, des études supplémentaires sont nécessaires pour démontrer l'efficacité des interventions.

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السياسات الغذائية الوطنية يف مجهورية إيران اإلسالمية الرامية إىل مكافحة األمراض غري السارية والوقاية منها معصومة مسلمي، مهرناز خرياندش، رامني نجاد فرد، هداية حسيني، هبروز جنات، وحيد مفيد، عاطف مقدم، نادر كريميان اخلالصة اخللفية: يلعب النظام الغذائي ً دورا ً مهاميف ُّالتعرضخلطر اإلصابة باألمراض غري السارية. ويف مجهورية إيران اإلسالمية، بدأت األنشطة الوطنية بعد إطالق خطة عمل منظمة الصحة العاملية بشأن الوقاية من األمراض غري السارية ومكافحتها. األهداف: هدفت هذه الدراسة إىل توضيح السياسات الغذائية الوطنية التي تنفذها احلكومة من أجل ِّ من احلداألمراض غري السارية يف البالد َو ْف ًقا خلطة عمل منظمة الصحة العاملية. طرق البحث: ُاستعرضت الدراسة املعايري واللوائح الغذائية َاملعتمدة ً حديثاواملتعلقة باألمراض غري السارية خالل الفرتة من 2013إىل 2018، كام متت مقارنة املستويات القصوى املسموح هبا من امللح والدهون ّاملتحولة والدهون َّاملشبعة يف املعايري القديمة واجلديدة. ُوق ِّمي توسيم إشارات املرور التغذوية إلذكاء الوعي العام ُّبالنظم الغذائية الصحية. النتائج: تم تقييم مخسة عرش ًمعيارا ًغذائيا ً مرتبطابثامنية أصناف غذائية ّتشكل ًحصة ًكبرية من سلة األغذية اإليرانية اليومية وثالثة أصناف ّتشكل ًحصةصغرية.وشملت السياسات اخلاصة بامللح خفض احلد األقىص للنسبة املئوية املسموح هبا يف اخلبز واجلبن واملرشوب ّ راملخم إىل %1 و3% و%0.8 عىل التوايل. وبالنسبة للدهون ّاملتحولة واملشبعة، ُح ِّددت النسب املئوية القصوى املسموح هبا عىل أهنا 2-5 % و30-65 % من الزيوت والدهون الصاحلة لألكل، عىل التوايل. وأصبح توسيم إشارات املرور التغذوية، الذي يشري إىل حمتوى امللح والسكر والدهون والدهون ّاملتحولة يف األغذية، ًإلزاميا جلميع األغذية منذ عام 2016. االستنتاجات:يف ضوء السياسات َّاملنفذةخلفض حمتوى امللح والدهون/ الزيوت يف األغذية، من املتوقع حدوث تراجع كبري يف األمراض غري السارية يف السنوات القادمة يف البلد. ومع ذلك، َث َّمة حاجة إىل مزيد من الدراسات إلثبات فعالية التدخالت.

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The status of cryptosporidiosis in Jordan: a review

AbdelRahman Zueter 1

1Department of Medical Laboratory Sciences, The Hashemite University, Zarqa, Jordan. (Correspondence to: AbdelRahman Zueter: zeuterabdelrah- [email protected]).

Abstract Background: Cryptosporidium is a waterborne intestinal parasite that causes diarrhoea in low and middle-income coun- tries worldwide. Reports from Mediterranean countries have documented the prevalence of cryptosporidiosis in children at various ages, also among cancer patients, and in cases of chronic kidney disease, haemodialysis, and organ transplant. Untill now, modified-acid staining preceded by stool concentration preparation remains the leading screening diagnostic test for the infection. In Jordan, few studies for cryptosporidiosis have been performed during the last 3 decades. Aims: This paper reviewed the status of cryptosporidiosis in Jordan and tracked recent updates for this emerging proto- zoal infection among different population groups. Methods: In this study, an online search was conducted on Google Scholar and PubMed databases using the keywords: Jordan, cryptosporidiosis and Cryptosporidium to inspect studies done on this parasite in Jordan. Results: Only 9 articles were identified from 1994 to 2019. These were analysed in terms of population group, demogra- phy, clinical history and the diagnostic tools used. Conclusion: Cryptosporidiosis is still neglected in Jordan as indicated by the low number of studies over the last 3 dec- ades and the prevalence is diverse depending on the diagnostic test used and socioeconomic status. Keywords: cryptosporidiosis, Jordan, diagnostic tools, identification Citation: Zueter A. The status of cryptosporidiosis in Jordan: a review. East Mediterr Health J. 2020;26(12):1565–1569. https://doi.org/10.26719/ emhj.20.065 Received: 27/09/19; accepted: 18/12/19 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Background Microscopic examination of stool using acid- fast staining, with or without stool concentration, is Cryptosporidium spp. are intracellular parasites of princi- the most frequently applied screening technique for pal concern, especially in some Mediterranean countries cryptosporidiosis. Acid-fast staining microscopy is with limited resources and in communities with low so- cheap and accessible in poor rural settings; it is the cioeconomic status (1,2). Globally, cryptosporidiosis has best parasitological method in terms of sensitivity and been ranked as the sixth most important foodborne para- specificity 14( ) and shows good performance when sitic infection of humans and domestic animals (3). compared with immunological and molecular methods Human cryptosporidiosis was first reported in 1976; (15). after that, it was identified as the major cause of chronic In Jordan, Cryptosporidium has been investigated diarrhoea in HIV-positive patients and children and as a either alone or along with other intestinal parasites in cause of zoonotic and waterborne diarrhoeal outbreaks various population groups (10,16), in the environment (4). Later, Cryptosporidium infection prevalence was seen (17) and in domestic animals (18). Prevalence ranges from to be on the rise among malnourished children and a 4% to 19%. Modified acid-fast staining microscopy has cause of premature death in low-resource settings (5–7). frequently been used as the diagnostic method of choice. Cryptosporidium is acquired mainly via contaminated Cryptosporidiosis risk factors have been reported in water and the ingested oocysts cause gastrointestinal Jordan, including drinking groundwater that is exposed symptoms before being shed in the stool and to contamination from sewage (17), immunosuppression transmitted to another host via the faecal–oral route (8). (10), contact with domestic animals and eating unwashed Cryptosporidiosis causes acute diarrhoea in children (9), vegetables (19,20). immunocompromised patients (3), cancer patients (10) This paper reviews the status of cryptosporidiosis and haemodialysis patients (11,12). The infection is usually in Jordan and tracks recent updates for this emerging self‑limiting in immunocompetent individuals, however, protozoal infection among different population groups. it might be life‑threatening in immunocompromised patients (2). The prevalence of cryptosporidiosis varies Literature review among different patient groups and this has been The search was performed on Google Scholar and Pu- attributed to the endemicity of the parasitic infection bMed databases using the keywords: Jordan, crypto- in the region of sampling along with environmental, sporidiosis and Cryptosporidium. Only 9 articles were climatic and sanitary factors (13). identified from 1994 until 2019 and were downloaded;

1565 Review EMHJ – Vol. 26 No. 12 – 2020 this reflects the scarcity of studies on this parasite in Jor- Cyclospora spp. and Cryptosporidium spp., Entamoeba dan. histolytica, Giardia lamblia, Blastocystis hominis, Endolimax The first study was published in 1994, it reported on nana, Hymenolepis nana and Ascaris lumbricoides. Bacteria the prevalence of various parasites in elementary school and other enteropathogens were also identified, including children in northern Jordan. Using various parasitological Salmonella spp., Shigella spp. and Escherichia coli. Oocysts of methods, Cryptosporidium spp. was detected in 40 out of Cryptosporidium spp. were observed in the samples from 1000 stool specimens collected from symptomatic and 16 (8%) patients, distributed as follows: 10 in children ≤ 14 asymptomatic elementary school children aged 6–14 years old (mean 7.5 years) and 6 in adults 15–87 years years in northern Jordan (16). The same study reported a (mean 51 years). Statistically significant risk factors for higher infection rate in the younger age group (< 9 years) the infection were related to the source of drinking water, than among children in the older age group, and a higher contact with animals and eating unwashed vegetables infection rate in villages than in cities. (16). (19). After that, and consistent with previous results Ten years later, 2 studies were published from the relating to Cryptosporidium prevalence, the same author same northern city; the first focused on drinking- further explored cryptosporidiosis in pre-school children water as a source of infection (17), while the second (less than 6 years old) who suffered from symptoms of study explored diagnostic methods, children groups, gastroenteritis and who were living in Irbid city, 85 km infection seasonality and source of drinking water (14). north of Amman, the capital of Jordan (20). In this study, Abo-Shehada et al. concluded that private groundwater Cryptosporidium oocysts were investigated using the reservoirs northern Jordan were significant enhancing formalin–ether concentration technique and cold acid- risk factors for contamination with C. parvum in rural fast staining followed by microscopy. Cryptosporidium villages (17). They postulated the source of contamination oocysts were detected in 6.7% (20 out of 300) of the was sewage disposal systems that were constructed near stool specimens collected from patients; 7/20 were also water reservoirs, which increased the risk of the leakage infected with other pathogens. Risk factors did not differ of their contents to be absorbed by the soil. Consequently, from those reported previously (16). However, it was there is a health hazard through the contamination noticed that breastfed children had a lower infection rate of drinking water stored in underground reservoirs. than those weaned early and those who were bottle-fed; Therefore, the underground location of water reservoirs this was attributed to passive maternal immunity as well must be considered to avoid groundwater–faecal as reduced exposure to contaminated water during bottle contamination. preparation (20). Another survey was done to investigate for Another study was done to explore different cryptosporidiosis among children from birth to 12 years intestinal parasites associated with diarrhoea in a rural at a hospital in Irbid (14). A single stool sample was area in the northeast of Jordan. The researchers collected collected from 300 children, 7 of whom were under 200 stool samples from patients with symptomatic chemotherapy treatment for cancer. This study compared gastroenteritis and these were examined using a number several diagnostic methods, including direct wet mount of parasitological methods including formalin–ethyl microscopy, flotation concentration, cold Kinyoun acetate concentration, wet preparation and modified Ziehl–Neelsen stain and direct immunofluorescence. acid-fast staining. Diagnosis revealed the oocysts of Oocysts were detected in 112 samples using direct

Table 1 Cryptosporidiosis in selected Mediterranean countries Country Population group Diagnostic method Prevalence (%) Reference Libya Diarrhoeal patients Lugol’s iodine, 4 22 aged 2–17 years immunofluorescence assay Egypt Children aged ≤ 8 years Nested-PCR 1.4 23 Lebanon Schoolchildren Modified Ziehl–Neelsen 10.4 24 staining and nested- PCR Palestine Gastroenteritis patients Malachite green Alla 25 (outbreak) negative staining and nested-PCR Egypt Adult Modified Ziehl–Neelsen 21 26 immunocompetent stain, sandwich ELISA, diarrhoeal patients nested-PCR Egypt Haemodialysis patients Cold modified Ziehl– 40 13 Neelsen staining

PCR = polymerase chain reaction. ELISA = enzyme-linked immunosorbent assay. aCryptosporidium detected in all outbreak cases.

1566 Review EMHJ – Vol. 26 No. 12 – 2020 immunofluorescence, which showed the highest the existence of a cryptosporidiosis outbreak during sensitivity and specificity, 100% and 98%, respectively. sampling. That study confirmed that chemotherapy A higher incidence rate was recorded during the rainy and immunosuppression are considered risk factors for season (January–May). Also, C. parvum was detected in cryptosporidiosis as suggested previously (14). the stools of 4 among the 7 paediatric oncology patients, The last published paper for cryptosporidiosis in Jordan suggesting an association of immune status as a risk was in October 2019 (12). This described the prevalence of factor (14). Overall, these results concur with previous cryptosporidiosis among haemodialysis patients from studies which indicated that contaminated drinking different areas. In that study a total of 133 stool samples water is a main source for the infection as well as the were collected and screened for Cryptosporidium oocyst increased incidence rate among rural areas (17,19,20). using formalin–ether concentration and a modified Molecular epidemiology has been extensively studied acid-fast staining technique. Cryptosporidium oocysts in the current decade to inspect common and new were recovered in 15/133 (11%) of the patients with higher genotypes of Cryptosporidium spp. in Jordan for a better positivity incidence reported in males and in rural understanding of the pathogen distribution, pathogenesis villages. The age of the patients ranged from 25 to 80 and transmission. Hijjawi et al. (21) genotyped 44 (mean 57.8; standard deviation 12.2) years and the most Cryptosporidium isolates from Jordanian children at the frequently reported symptoms were gastrointestinal 18S rRNA locus and identified 4Cryptosporidium spp.: C. symptoms. The study ensured the importance of parvum (n = 22), C. hominis (n = 20), C. meleagridis (n = 1) modified acid-fast stain as a primary screening method and C. canis (n = 1). Furthermore, subtyping for 29 isolates and has recommended increasing the awareness of this at the 60-kDa glycoprotein (GP60) locus revealed several parasite in this population group, and to include patients rare and novel subtypes indicating unique endemicity with kidney transplantation as well (12). and transmission of Cryptosporidium in Jordan. The Reports for cryptosporidiosis from Jordan among same study showed that quantitative polymerase chain different population groups relatively concurs with those reaction (qPCR) increased the sensitivity of detection and from neighbouring and countries and other countries in confirmed the prevalence of the infection at up to 19% the Region, which reflects the endemicity of this parasite instead of the 1.8% that was obtained using microscopy. and the need for more extensive epidemiological studies. Another genotyping study expanded the targeted Table 1 summarizes selected studies on cryptosporidiosis, populations to include several kinds of animals besides highlighting the status of cryptosporidiosis in other humans since associations of animals as a probable risk Mediterranean countries and illustrating the diversity of factor for cryptosporidiosis was postulated previously diagnostic methods applied as well as the variation in the (16,19). A total of 284 stool samples from Jordanian cattle, prevalence among these countries, all of which indicates sheep, goats and chickens and 48 human stool samples the relative harmony between these reports and the were screened via 18S-qPCR and lectin locus-specific results and methods reported in Jordan. qPCR. The age of the humans sampled ranged from 10 Conclusion months to 56 years and all were immunocompetent, hospitalized with a history of diarrhoea, abdominal pain Cryptosporidiosis is still neglected in Jordan as indicated and gastroenteritis. Cryptosporidium DNA was amplified by the low number of studies over the last 3 decades and in 37/284 (13.0%) of animal and 4/48 (8.3%) of human the prevalence is diverse depending the applied diagnos- samples. Speciation revealed 6 different Cryptosporidium tic test and the socioeconomic status. species, including C. xiaoi, C. andersoni, C. ryanae, C. Recommendations parvum, and C. baileyi. The study identified several novel and previously existing subtypes for C. parvum isolates at Extensive studies on cryptosporidiosis in Jordan should the 60-kDa glycoprotein (gp60) obtained from humans be conducted and may include patients with the fol- and animals (18). lowing inclusion criteria: kidney transplantation, auto- immune disorders, immunocompetent and immuno- Another genetic study was done in 2017 and assessed compromised children and adults, gastroenteritis, low the prevalence and genotypes of Cryptosporidium among socioeconomic status, from rural areas of different loca- paediatric oncology and non-oncology patients (10). In tions in Jordan, and people depending on groundwater for brief, Hijjawi et al. reported a statistically significantly drinking. Modified acid-fast staining is informative and higher prevalence of cryptosporidiosis (14.4%; 23 out of less expensive as a diagnostic screening tool in Jordan. 160) among symptomatic paediatric oncology patients Development, validation, and evaluation of Cryptosporid- than symptomatic paediatric nononcology patients ium–stool antigen immunoassay might be successful in (5.1%; 7 out of 137) using the modified acid-fast stain increasing the specificity and sensitivity of detection and (10). All microscopy-positive stools were introduced in reducing the costs in comparison with PCR. Finally, for DNA extraction and were genotyped at species and gp60 genotyping is important to investigate and track subtype levels using the 18S and gp60 loci, respectively. suspected common-source Cryptosporidium outbreaks. Cryptosporidium parvum was identified in all samples. Clustering of the same subtype (IIaA17G2R1) was noticed Funding: None. in almost all species from the 2 patient groups, suggesting Competing interests: None declared.

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Bilan de la situation de la cryptosporidiose en Jordanie Résumé Contexte : Cryptosporidium est un parasite intestinal d’origine hydrique qui provoque des diarrhées et que l’on retrouve dans les pays à revenu faible et intermédiaire du monde entier. Des rapports provenant de pays méditerranéens ont mis en évidence les taux de prévalence de la cryptosporidiose chez les enfants appartenant à divers groupes d’âge, les personnes atteintes de cancer ou d’insuffisance rénale chronique et les personnes ayant subi une hémodialyse ou une greffe d’organe. La coloration acido-résistante modifiée d’une préparation de selles concentrées reste à ce jour le principal test diagnostique utilisé pour le dépistage de l’infection. Peu d’études sur la cryptosporidiose ont été réalisées en Jordanie au cours des trois dernières décennies. Objectifs : La présente étude visait à examiner la situation de la cryptosporidiose en Jordanie et à suivre les mises à jour récentes concernant cette infection à protozoaire émergente dans différents groupes de population. Méthodes : Dans la présente étude, une recherche a été réalisée en ligne sur les bases de données Google Scholar et PubMed. Les mots clés suivants ont été utilisés : Jordanie, cryptosporidiose et Cryptosporidium. L’objectif était de recenser les études réalisées sur ce parasite en Jordanie. Résultats : Seuls neuf articles publiés entre 1994 et 2019 ont été recensés. Les éléments suivants ont été analysés : groupe de population, démographie, histoire clinique et outils diagnostiques utilisés. Conclusion : La cryptosporidiose est encore négligée en Jordanie, comme l’indique le faible nombre d’études réalisées au cours des trois dernières décennies. La prévalence varie par ailleurs selon le test diagnostique utilisé et le statut socio- économique.

حالة داء َخ ِفيات األبواغ يف األردن: استعراض عبد الرمحن زعيرت اخلالصة اخللفية: خفية األبواغ هو طفييل َم َعوي ينتقل عن طريق املاء ُويسبب اإلسهال يف البلدان النامية واملتخلفة يف مجيع أنحاء العامل. وقد َّوثقت تقارير واردة من بلدان البحر املتوسط انتشار داء خفيات األبواغ بني األطفال يف خمتلف األعامر، ًبني وأيضامرىض الرسطان، ويف حاالت أمراض ُالك َل املزمنة، وغسيل ُالك َل، وزرع األعضاء. وحتى اآلن، ال يزال التلوين باحلمض ُامل َّ ل عدالذي يسبقه إعداد تركيز الرباز هو االختبار التشخييص الرئييس ُ ِّللتحري عن العدوى. وأجريت يف األردن بعض الدراسات عن داء خفيات األبواغ خالل الثالثة عقود املاضية. األهداف:هدفت هذه الدراسة إىل بحث حالة داء خفيات األبواغ يف األردن، وتتبع آخر مستجدات عدوى األوايل الناشئة بني خمتلف الفئات السكانية. طرق البحث: ُجري أبحث عرب اإلنرتنت يف إطار هذه الدراسة عل قاعديت بيانات Google Scholar و PubMedباستخدام الكلامت الرئيسية التالية: األردن، داء خفيات األبواغ، خفية األبواغ، الستقصاء الدراسات التي ُأجريت عل هذا الطفييل يف األردن. النتائج: ُح ِّددت 9 مقاالت فقط يف الفرتة من عام 1994 إىل عام . 2019وجرى حتليلها من حيث الفئة السكانية، والوضع السكاين، والسوابق الرسيرية، واألدوات التشخيصية َاملستخدمة. االستنتاجات: ال يزال داء خفيات األبواغ ًيف مهمالاألردن، ويشري إىل ذلك انخفاض عدد الدراسات التي ُأجريت بشأنه عل مدى العقود الثالثة املاضية، ويتفاوت معدل االنتشار ًاعتامدا عل االختبار التشخييص َاملستخدم واحلالة االجتامعية االقتصادية.

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Implementing the Health Early Warning System based on syndromic and event-based surveillance at the 2019 Hajj

Kingsley Lezor Bieh,1 Anas Khan,1,2 Saber Yezli,1 Ahmed El-Ganainy,1 Sari Asiri,3 Badriah Alotaibi,3 Sujoud Ghallab,1 Amgad Elkholy,4 Abdinasir Abubakar 4 and Hani Jokhdar 3

1Global Center for Mass Gatherings Medicine (WHO Collaborating Center for Mass Gatherings Medicine) Ministry of Health, Riyadh, Saudi Arabia. 2Emergency Medicine Department, College of Medicine, King Saud University, Riyadh, Saudi Arabia. 3Ministry of Health, Riyadh, Saudi Arabia. 4World Health Organization Eastern Regional Office for the Eastern Mediterranean, Cairo, Egypt. (Correspondence to: Kingsley Lezor Bieh: [email protected]. sa; [email protected]).

Abstract Background: During the 2019 Hajj, the Ministry of implemented for the first time a health early warning system for rapid detection and response to health threats. Aims: This study aimed to describe the early warning findings at the Hajj to highlight the pattern of health risks and the potential benefits of the disease surveillance system. Methods: Using syndromic surveillance and event-based surveillance data, the health early warning system generated automated alarms for public health events, triggered alerts for rapid epidemiological investigations and facilitated the monitoring of health events. Results: During the deployment period (4 July–31 August 2019), a total of 121 automated alarms were generated, of which 2 events (heat-related illnesses and injuries/trauma) were confirmed by the response teams. Conclusion: The surveillance system potentially improved the timeliness and situational awareness for health events, including non-infectious threats. In the context of the current COVID-19 pandemic, a health early warning system could enhance case detection and facilitate monitoring of the disease geographical spread and the effectiveness of control meas- ures. Keywords: syndromic surveillance, event-based surveillance, early warning, Hajj, mass gathering, pilgrim Citation: Bieh KL; Khan A; Yezli S; El-Ganainy A; Asiri S; Alotaibi B; et al. Implementing the Health Early Warning System based on syndromic and event-based surveillance at the 2019 Hajj. East Mediterr Health J. 2020;26(12):1570–1575. https://doi.org/10.26719/emhj.20.129 Received: 18/05/20; accepted: 11/06/20 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Background pre-diagnostic data analysis; it captures unstructured data from diverse settings, including health care, media In August 2019, 2 489 406 Muslim pilgrims, of which and community settings, to trigger public health alert 74.5% were international pilgrims, performed the 2019 and response (9). (1440) Hajj in Makkah, Saudi Arabia. Over half (55.6%) of all pilgrims were males, and 9.2% of pilgrims were Saudi The systematic real-time (or near real-time) reporting nationals (excludes non-Saudi residents) (1). of both syndromic surveillance and EBS data thus provides an opportunity for early warning, especially in Disease prevention and control remains a national, an international mass gathering context where timely regional and international public health priority during detection and response is required for prompt risk Hajj (2,3). Among various interventions, the deployment mitigation and prevention. In addition, the ongoing of enhanced disease surveillance system is recommended systematic collection and analysis of surveillance for mass gatherings to facilitate rapid detection and data could improve situational awareness, provide response to health threats (4). A case-based infectious reassurance of the absence of public health threats and diseases surveillance system, which uses an electronic guide continuing public health decision making (4,7). portal for rapid data management, is deployed for Hajj Given these potential benefits, the Ministry of Health (5). However, the focus on specific infectious threat is a in Saudi Arabia implemented a health early warning recognized limitation of the surveillance system (6). system (HEWS) during the 2019 (1440) Hajj. The health Syndromic and event-based surveillance (EBS) early warning system used both syndromic and EBS systems complement routine case-based surveillance data to rapidly detect potential public health threats, systems in mass gatherings settings (4,7). By using triggered corresponding alerts for rapid epidemiological data that precede diagnostic confirmation, syndromic investigations and monitored the trend of confirmed surveillance facilitates prompt detection of existing health events during the 2019 (1440) Hajj. This study threats, improves the surveillance for emerging diseases aims to describe the early warning findings at the Hajj and provides an opportunity for rapid response (4,8). to highlight the pattern of health risks and the potential Event-based surveillance also ensures timeliness through benefits of the disease surveillance system.

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Methods the period of Hajj rites (9–14 August 2019), and 80.2% of the total consultations during this period were among This study is a descriptive analysis of surveillance data pilgrims (Figure 1). from the HEWS implementation processes during the 2019 Hajj. The projected target coverage of HEWS is Males represented 54.4% of all consultations and at least 80% of health facilities (hospitals and primary 62.8% of those among pilgrims. The proportion of health centres), but coverage was limited to only Minis- consultations for each age group of pilgrims were 50% try of Health hospitals in 2019. The included syndromes (45-64 years), 29.6% (25–44 years), 14.9% (≥ 65 years) and and events were identified through an international 4.9% (≤ 24 years). technical consultation organized by the World Health During the deployment period, 121 automated Organization (WHO) and the Ministry of Health (Table alarms were generated for the following syndromes: 1). A web-based electronic solution, which was anchored acute febrile syndrome without rash (60), severe acute on an existing information exchange and data analytic respiratory infections (18), acute febrile syndrome with tool, was developed for HEWS data management. Rele- neurological manifestation (14), acute febrile syndrome vant data were pooled from hospital electronic medical with rash (10), heat-related illnesses (HRI) (10), acute records (EMRs) and integrated in a central database to jaundice syndrome (7), and chemical injuries (2). Of these, provide a unified data source. 49 field investigations were conducted and an additional The raw data, including the International alert was issued for trauma/injuries based on analysis Classification of Diseases (ICD) 10 provisional diagnosis, of a hotline-generated event, in the aftermath of an were extracted and read periodically (hourly) from the unexpected heavy rainfall in the Hajj areas. central database, and then applied with the defined logic The response team confirmed two health events for priority syndromes and events to generate automated (HRI and trauma/injuries) as depicted in Figure 2. The alarm on the HEWS dashboards. Additionally, a hotline suspected HRI cases included citizens of 56 countries. was established for the report of public health events Furthermore, females represented 46.7% of suspected directly to the Command Centre. Initial alarm thresholds HRI cases and the majority (79%) were reported from were set based on the benchmarks in a WHO regional Arafat and Mina hospitals. The trauma/injury cases syndromic surveillance system and the moving average mostly involved males (66.7%), and the age group statistical algorithms (8). Each alarm was reviewed by distribution of cases were <15years (2.08%), 15–24years two epidemiologists before an alert was issued for field (12.5%), 25–44years (36.45%), 45–64years (29.16%), investigation. Response was integrated with those of the >64years (9.37%) and missing (10.41%). The peak daily pre-existing enhanced infectious disease surveillance mean response time (period between a public health alert system for Hajj (5,6). The dissemination of this and report of event status by investigation teams). was surveillance finding is approved by the Saudi Ministry of 3.44 hours and the lowest daily mean response time was Health surveillance team. Supplementary data will only 1.47 hours. No other priority syndromes or health events be shared on request after a review by the surveillance were detected by HEWS and no cases of priority diseases team. were reported by the pre-existing surveillance system from the HEWS reporting sites. Results The surveillance data was reported from the emergen- Discussion cy and outpatient departments of 16 Ministry of Health The health early warning system improved the timeli- hospitals. A total of 409 098 consultations (62.18% among ness of reporting and detected two non-infectious health non-pilgrims) were reported during the deployment pe- risks during the 2019 Hajj. The development and linkage riod. The number of daily consultations peaked during of HEWS with pre-existing data management technolo-

Table 1 List of priority syndromes and events Syndromes Events Acute febrile syndrome without rash Food poisoning Acute febrile syndrome with rash Heat-related illness Acute febrile syndrome with neurological manifestation Chemical, biological, radiological and nuclear emergencies Acute jaundice syndrome Trauma/injuries Acute flaccid paralysis (AFP) Cluster of cases or unusual health events Acute haemorrhagic fever Detection of unusual pathogens Severe acute respiratory infections – Acute respiratory distress syndrome – Acute watery diarrhoea – Acute bloody diarrhoea –

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Figure 1 Graphical representation of the total number of consultations and reporting sites

25000 26 24 22 2000 20 18 15000 16 14 12 10000 10

Number of consultations of Number 8 6 5000

4 sites) hospitals (reporting of Number 2 0 0 04 - Jul - 19 04 - Jul - 19 06 - Jul - 19 08 - Jul - 19 10 - Jul 12 - 19 - Jul - 19 14 - Jul - 19 16 - Jul - 19 - Jul 18 - 19 20 - Jul - 19 22 - Jul - 19 24 - Jul - 19 - Jul 26 - 19 - Jul 28 - 19 30 - Jul 01 - Aug - 19 03 - Aug - 19 05 - Aug - 19 07 - Aug - 19 09 - Aug - 19 11 - Aug - 19 - Aug - 19 13 15 - Aug - 19 - Aug - 19 17 - Aug 19 - 21 - Aug - 19 23 - Aug - 19 23 25 - Aug - 19 27 - Aug - 19 29 - Aug - 19 31 - Aug - 19

Hajj patients Non-Hajj patients Number of hospitals gy within the Ministry of Health promoted the effective purposes ensured that additional data collection tasks use of available resources. In addition, the use of sec- were not assigned to already over-burdened health-care ondary data captured primarily for clinical consultation professionals in Hajj. Similar principles informed the

Figure 2 Epi-curve of confirmed priority health events during the 2019 Hajj

120

Heat syncope Heat fatigue, transient 100 Effect of heat and light Heat stroke Heat exhaution 80 Unspecified fall

60 Number of cases of Number

40

20

0 31 - Jul 1 - Aug 2 - Aug- 2 Aug- 3 4 - Aug 5 - Aug Aug- 7 8 - Aug 9 - Aug 6 - Aug 10 - Aug 11 - Aug 12 - Aug 15 - Aug 13 - Aug 13 14 - Aug 16 - Aug - Aug18 - Aug 19 17 - Aug 17 20 - Aug 21 - Aug

1572 Short research communication EMHJ – Vol. 26 No. 12 – 2020 use of existing data in other mass gatherings syndromic and ensure that data sharing occurs in a highly secured surveillance systems (10,11). Electronic data management virtual environment. Under the International Health is fast becoming an integral part of most early warning Regulation (IHR 2005), countries ought to implement systems due to the benefits of promoting timeliness of and maintain functional EBS and indicator-based reporting, and minimizing the significant manpower surveillance systems to meet the target for enhanced needs and human errors that are often associated with surveillance capacity (17). Expanding HEWS as a national manual data management (10). disease surveillance system would contribute to meeting The number of automated alarms increased with daily this global health security target. consultation rates, and nearly half of all generated alarms were made for acute febrile syndrome. Indeed, fever Limitations unspecified was among the leading ICD 10 provisional As a limitation, the periodic (hourly) data extraction from diagnosis at the 2019 Hajj, and the variation in number the central database rendered HEWS a near real-time sur- of cases had no major public health implication. Since veillance system. In non-mass gatherings settings, this a missed event in the Hajj could have profound health hourly time-lag may be nearly insignificant. However, security impacts, the setting of HEWS notification thresholds favoured increased sensitivity of the in reality some pilgrims depart from the health facility system and by implication the number of false alarms. within one hour of their arrival for a consultation visit. In Anticipating the stretch of field response resources, the a crowded setting where pilgrims are constantly mobile dashboard verification of automated alarms reduced the and have no stable addresses, identifying cases before number of investigation alerts by more than half. they depart from the health-care facility is both logistical- The detected health events (HRI and injuries) were ly desirable and risks mitigating during response. How- monitored and controlled with appropriate mitigating ever, nearly all response feedbacks were received within measures, including redeployment of manpower the stipulated period (6 hours) to guide ongoing deci- resources. While the number of suspected HRI cases sion-making, primarily due to the linkage of HEWS with declined sharply after an initial peak on the Day of Arafat the response resources of the pre-existing surveillance (11 August) due to an unexpected heavy rainfall, more system. Preliminary validation reports showing around pilgrims were injured from falls on the wet slippery 10–20% of missing data in the central database may have surfaces. In contrast to sporting mass gatherings where compromised the quality of HEWS data. The finding of injuries often arise from athletic activities, the risk of incomplete entries by physicians is consistent with those injuries in the Hajj is predominantly heightened by crowd- of other similar disease surveillance systems (10,18). Addi- related incidents (3,12). Heat-related illnesses are among tionally, potential public health threats, particularly less the leading causes of morbidity and mortality at the Hajj, severe cases presenting to primary health centres, could when the pilgrimage is held during the summer months have been missed since the system coverage was limited (13–15). The HEWS surveillance finding is consistent with to 16 Ministry of Health hospitals in the Hajj areas. How- historical data regarding the geographical distribution ever, there were no reports of any major health threats of HRI cases during Hajj (13,14). A plausible reason for the high HRI disease burden in Mina and Arafat is the from the pre-existing infectious disease surveillance intensified physical exertion and increased exposure of system, which had a broader coverage. pilgrims to hot weather as they perform the required Hajj Conclusion rites in mostly open and unsheltered areas. In future Hajj seasons, HEWS aims to capture data This study provides valuable insight into the benefits from at least 80% of all health facilities and incorporate of an early warning system in an international mass non-facility based reporting sites, such as internet and gathering context, with prevalent global health security social media platforms and over-the-counter drug sales risks. It potentially improves timeliness and the situa- records. Studies have shown that non-health facility based tional awareness for health events, including non-in- data collection improves the timeliness of syndromic fectious threats. In the context of the current COVID-19 surveillance systems (9,16). Conceivably, the cooperation pandemic, HEWS could enhance case detection and fa- of countries sending pilgrims to the Hajj, especially cilitate monitoring of the disease geographical spread countries setting up clinics to assist in providing care for and the effectiveness of control measures. their own pilgrims, is needed for the integration of their None. health clinics to the HEWS database. To achieve this, the Funding: Ministry of Health would set interoperability standards Competing interests: None declared.

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Mise en œuvre du système d'alerte sanitaire précoce basé sur la surveillance syndromique et fondée sur les événements lors du Hadj de l’année 2019 Résumé Contexte : Au cours du Hadj de l’année 2019, le Ministère de la Santé d'Arabie saoudite a mis en place pour la première fois un système d'alerte précoce en matière de santé pour une détection des menaces sanitaires et une riposte rapides face à celles-ci. Objectifs : La présente étude avait pour objectif de présenter les résultats de l'alerte précoce lors du Hadj afin de mettre en évidence le schéma des risques sanitaires et les avantages potentiels du système de surveillance des maladies. Méthode : À l’aide de la surveillance syndromique et des données de surveillance basée sur les événements, le système d'alerte sanitaire précoce a généré des alarmes automatisées pour les événements de santé publique, a déclenché des alertes en vue d’enquêtes épidémiologiques rapides et a facilité le suivi des événements de santé. Résultats : Au cours de la période de déploiement (4 juillet-31 août 2019), un total de 121 alarmes automatiques ont été générées, dont deux événements (maladies et blessures/traumatismes liés à la chaleur) ont été confirmés par les équipes d’intervention. Conclusions : Le système de surveillance a potentiellement amélioré la notification en temps voulu des événements de santé et la connaissance des situations concernant ces événements, y compris les menaces non infectieuses. Dans le contexte de la pandémie actuelle de COVID-19, un système d'alerte précoce permettrait d’améliorer la détection des cas et de faciliter le suivi de la propagation géographique de la maladie ainsi que l'efficacité des mesures de lutte.

تنفيذ نظام اإلنذار الصحي املبكر القائم عىل ترصّد املتالزمات واألحداث يف موسم احلج لعام 2019 كينجسيل لزور بيه، أنس خان، صابر يزيل، أمحد اجلنايني، ساري عسريي، بدرية العتيبي، سجود غالب، أجمد اخلويل، عبدي-نارص أبو بكر، هاين جوخضار اخلالصة اخللفية: َن ّفذت، ألول مرة، وزارة الصحة يف اململكة العربية السعودية، خالل موسم احلج لعام 2019، ًنظاما لإلنذار املبكر للكشف الرسيع عن األخطار الصحية واالستجابة هلا. األهداف: هدفت هذه الدراسة إىل وصف نتائج اإلنذار املبكر يف موسم احلج لتسليط الضوء عىل نمط املخاطر الصحية والفوائد املحتملة لنظام ّترصد األمراض. طرق البحث: أصدر نظام اإلنذار الصحي املبكر، باستخدام بيانات ّترصد املتالزمات واألحداث، إنذارات آلية ألحداث صحية عامة، وأطلق تنبيهات إلجراء استقصاءات وبائية رسيعة، وي ّرس رصد األحداث الصحية. النتائج: خالل فرتة النرش ) 4يوليو/متوز - 31 أغسطس/آب 2019(، صدر ما جمموعه 121 ًإنذارا ًآليا، وأكدت فرق االستجابة حدثني منها )أمراض مرتبطة باحلرارة وإصابات/ورضوح(. االستنتاجات: ُحي َت َمل أن ّ نحيس نظام ّالرتصد التوقيت والوعي بأوضاع األحداث الصحية، ومن ضمنها التهديدات غري املعدية. ويف سياق جائحة كوفيد19- احلالية، يمكن لنظام اإلنذار الصحي املبكر أن يعزز اكتشاف احلاالت ويي ّرسرصد االنتشار اجلغرايف لألمراض وفعالية تدابري املكافحة.

References 1. General Authority of Statistics. Hajj Statistics, Kingdom of Saudi Arabia, 2019. Riyadh: General Authority of Statistics; 2019 (https://www.stats.gov.sa/en/28). 2. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). WHO statement on successful con- clusion of hajj 1440/2019. Cairo: WHO/EMRO; 2019 (http://www.emro.who.int/media/news/who-statement-on-successful-conclu- sion-of-hajj-14402019.html). 3. Memish ZA, Steffen R, White P, Dar O, Azhar EL, Sharma A, et al., Mass gatherings medicine: public health issues arising from mass gathering religious and sporting events. Lancet. 2019;393(10185):2073-2084. 4. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Public health for mass gatherings: key considerations. Cairo: WHO/EMRO; 2015. 5. Memish ZA, Zumla A, Alhakeem RF, Assiri A, Turkestani A, Al-Harby KD, et al. Hajj: infectious disease surveillance and control. The Lancet. 2014;383(9934):2073-2082.

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6. Alotaibi BM, Yezli S, Bin Saeed A-AA, Turkestani A, Alawam AH, Bieh KL Strengthening health security at the Hajj mass gatherings: characteristics of the infectious diseases surveillance systems operational during the 2015 Hajj. J Travel Med. 2017;24(3):taw087. 7. McCloskey B, Endericks T, Catchpole M, Zambon N, Mclauchlin J, Shetty N, et al. London 2012 Olympic and Paralympic Games: public health surveillance and epidemiology. The lancet. 2014;383(9934):2083-2089. 8. Triple S – Guidelines for designing and implementing a syndromicsSurveillance system. Paris: French Institute for Public Health Surveillance; 2013. 9. Keller M, Blench M, Tolentino H, Friefeld CC, Mandl K, Mawudeku A, et al. Use of unstructured event-based reports for global infectious disease surveillance. Emerg Infect Dis. 2009;15(5):689. 10. Elliot AJ, Hughes HE, Hughes TC, Locker TE, Shannon T, Heyworth J, et al. Establishing an emergency department syndromic surveillance system to support the London 2012 Olympic and Paralympic Games. Emerg Med J. 2012;29(12):954-960. 11. Williams CJ, Schenkel K, Eckmanns T, Altmann D, Krause G. FIFA World Cup 2006 in Germany: enhanced surveillance improved timeliness and detection. Epidemiol Infect. 2009;137(4):597-605. 12. Yancey AH, Fuhri PD, Pillay Y, Greenwald I., et al., World Cup 2010 planning: an integration of public health and medical systems. Public Health. 2008;122(10):1020-9. 13. Khogali M. Epidemiology of heat illnesses during the Makkah Pilgrimages in Saudi Arabia. Int J Epidemiol. 1983;12(3):267-273. 14. Abdelmoety DA, El-Bakri NK, Almowalld WO, Turskestani ZA, Bugis BA, Baseif E, et al. Characteristics of heat illness during Hajj: a cross-sectional study. Biomed Res Int. 2018;2018:5629474. 15. Ministry of Health. Statistics Year Book 1438H, Ministry of Health, Kingdom of Saudi Arabia. Riyadh: Ministry of Heath; 2018 (https://www.moh.gov.sa/en/Ministry/Statistics/book/Pages/default.aspx). 16. Hogan WR, Tsui F-C, Ivanov O, Gesteland P, Grannis S, Overhage J, et al., Detection of pediatric respiratory and diarrheal out- breaks from sales of over-the-counter electrolyte products. J Am Med Inform Assoc. 2003;10(6):555-562. 17. World Health Organization, International Health Regulations (IHR): Joint External Evaluation (JEE): country Implementation guide. Geneva: World Health Organization; 2017. 18. Napoli C, Riccardo F, Declich S, Dente M, Pompa M, Rizzo C, et al., An early warning system based on syndromic surveillance to detect potential health emergencies among migrants: results of a two-year experience in Italy. Int J Environ Res Public Health. 2014;11(8):8529-8541.

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Elimination of neglected tropical diseases under preventive chemotherapy programmes in the Eastern Mediterranean Region1

Citation: Elimination of neglected tropical diseases under preventive chemotherapy programmes in the Eastern Mediterranean Region. East Mediterr Health J. 2020;26(12):1576–1577 https://doi.org/10.26719/2020.26.12.1576 Copyright © World Health Organization (WHO) 2020. Open Access. Some rights reserved. This work is available under the CC BY-NC-SA 3.0 IGO license (https://creativecommons.org/licenses/by-nc-sa/3.0/igo).

Introduction schistosomiasis, onchocerciasis, soil-transmitted helminthiasis and trachoma in the Region; The World Health Organization (WHO) global and re- gional preventive chemotherapy programmes have • present the WHO NTD roadmap 2030 and discuss its made a number of key accomplishments. These include adaptation to country context and the development of the elimination of lymphatic filariasis as a public health country-specific NTD plans for 2021–2030; and problem in Yemen and the establishment of public–pri- • discuss country-specific plans of action for 2020, vate partnerships to facilitate progress towards the elim- including drug requirements, to provide input and ination and control of neglected tropical diseases (NTDs) recommendations on their funding, design and (1). More than 1 billion people had been treated globally in implementation. 2018 for at least one of five NTDs targeted for control and Summary of discussions elimination, with over 1.7 billion treatments distributed to populations in need through mass drug administra- A global update on NTDs was presented along with pro- tion (MDA) and a regional coverage of preventive chemo- gress towards achieving NTD targets in the Eastern Med- therapy of 21.4% (2). iterranean Region (EMR). In 2017, the size of the popu- lation in the EMR requiring interventions against NTDs As an important step in paving the way to end was estimated at 10 million less than in 2016, mainly due the epidemics of NTDs by 2030, the 18th meeting to the reduction of soil-transmitted helminthiasis preva- of the Regional Programme Review Group (RPRG) lence in some areas of Sudan as indicated by a prevalence on elimination of neglected tropical diseases under survey conducted in 2017. In addition, The Egyptian Min- preventive chemotherapy programmes in the WHO istry of Health and Population has accelerated elimina- Eastern Mediterranean Region was convened by the WHO tion of schistosomiasis (commonly known as bilharzia- Regional Office for the Eastern Mediterranean in Sharm sis) by earmarking an equivalent of US$ 2 million a year 3 El Sheikh, Egypt, 9–11 December 2019 ( ). The meeting was for a period of five years 4( ). attended by the members of the RPRG, representatives from the ministries of health of Afghanistan, Djibouti, The NTD Roadmap 2021–2030 was presented, which Egypt, Iraq, Morocco, Pakistan, Saudi Arabia, Somalia, is a high-level global strategy that will set the overall Sudan, Syrian Arab Republic, Tunisia and Yemen. direction for the fight against NTDs, tailored to a diverse Representatives of partner organizations, including the set of audiences. The content of the roadmap was Expanded Special Project for Elimination of Neglected outlined, including the milestones for overarching and Tropical Diseases (ESPEN), Mectizan Donation Program, cross-cutting targets, the disease-specific targets and an Sightsavers and United Nations Relief and Works Agency analysis of those areas requiring strengthening across multiple diseases. for Palestine Refugees in the Near East (UNRWA) also attended the meeting. The process of validation of trachoma elimination as a public health problem was discussed. In addition, The objectives of the meeting were to: the WHO Joint Application Package for preventive • review country-specific progress made during 2018 chemotherapy was presented and common mistakes, and 2019 by preventive chemotherapy programmes challenges and shortfalls when preparing the Joint for NTDs to track the progress made towards Reporting Forms and Joint Request for Selected achieving the NTD milestones and targets included Medicines were explained. in the roadmap for WHO’s work in the Eastern Mediterranean Region, discuss challenges in Recommendations implementation and identify solutions; To WHO • update participants on the current situation, • Providing technical support and capacity-building to innovations and challenges for control and elimination countries for developing/updating NTD elimination of NTDs, with a focus on lymphatic filariasis, and control plans and for their implementation;

1 This summary is extracted from the Summary report on the Eighteenth meeting of the Regional Programme Review Group on the elimination of neglected tropical diseases under preventive chemotherapy programmes in the Eastern Mediterranean Region, Sharm el Sheikh, Egypt, 9–11 December 2019 (https://applications.emro.who.int/docs/WHOEMCTD083E-eng.pdf?ua=1).

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• assisting countries to identify local research priorities To Member States for overcoming operational challenges; • Strengthening national NTD control/elimination • advocating for NTD programmes and resource programmes and having focal persons at national and mobilization initiatives with senior health and subnational levels to coordinate activities; finance ministry officials to ensure the allocation of • establishing a multisectoral coordination mechanism/ resources from domestic funding and partners; committee for NTDs, including representation from • maintaining annual RPRG/programme managers’ relevant sectors and stakeholders, such as the finance, meetings to provide an opportunity for Member education and water, sanitation and hygiene sectors; States to obtain new information, learn best practices • integrating NTD interventions within existing and share experiences with all stakeholders, including health programmes that receive substantial funding donors; and support; and • facilitating cross-border collaboration and • developing a compelling evidence-based investment coordination between neighbouring countries and case that NTD elimination and control supporting regions, where appropriate. inclusion within national health plans and policy.

References 1. World Health Organization. Despite challenges, Yemen eliminates lymphatic filariasis. Geneva: World Health Organization; 2019 (https://www.who.int/neglected_diseases/news/yemen-eliminates-lymphatic-filariasis/en/). 2. World Health Organization. Neglected tropical diseases: treating over one billion people for the fourth successive year. Geneva: World Health Organization; 2019 (https://www.who.int/neglected_diseases/news/treating-over-one-billion-people-for-the-fourth- successive-year/en/). 3. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Eighteenth meeting of the Region- al Programme Review Group on the elimination of neglected tropical diseases under preventive chemotherapy programmes in the Eastern Mediterranean Region, Sharm el Sheikh, Egypt, 9–11 December 2019 (https://applications.emro.who.int/docs/ WHOEMCTD083E-eng.pdf?ua=1). 4. World Health Organization. Egypt leverages domestic funding to eliminate schistosomiasis. Geneva: World Health Organiza- tion; 2016 (https://www.who.int/neglected_diseases/news/Egypt_leverages_domestic_funding_to_eliminate_schistosomiasis/ en/).

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