Eastern Mediterranean La Revue De Santé De La Health Journal Méditerranée Orientale

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

Nurses make up the largest group of health-care providers and are the first point of contact in health service delivery of diabetes in terms of detection, treatment and rehabilitation. This year’s World Diabetes Day coincides with the International Year of the Nurse and the Midwife, as designated by the World Health Assembly, and looks to focus on and promote the role of nurses in the prevention and management of diabetes.

المجلد السادس والعشرون / عدد Volume 26 / No. 11 2020 11 نوفمبر/تشرين الثاني November/Novembre Eastern Mediterranean Health Journal Members of the WHO Regional Committee for the Eastern Mediterranean IS the official health journal published by the Eastern Mediterranean Regional Office of the World Health Organization. It is a forum for Afghanistan . Bahrain . Djibouti . Egypt . Islamic Republic of Iran . Iraq . Jordan . Kuwait . Lebanon the presentation and promotion of new policies and initiatives in public health and health services; and for the exchange of ideas, concepts, Libya . Morocco . Oman . Pakistan . Palestine . Qatar . Saudi Arabia . Somalia . Sudan . Syrian Arab Republic epidemiological data, research findings and other information, with special reference to the Eastern Mediterranean Region. It addresses Tunisia . United Arab Emirates . Yemen all members of the health profession, medical and other health educational institutes, interested NGOs, WHO Collaborating Centres and individuals within and outside the Region. البلدان أعضاء اللجنة اإلقليمية ملنظمة الصحة العاملية لرشق املتوسط املجلة الصحية لرشق املتوسط األردن . أفغانستان . اإلمارات العربية املتحدة . باكستان . البحرين . تونس . ليبيا . مجهورية إيران اإلسالمية هىاملجلة الرسمية التى تصدر عن املكتب اإلقليمى لرشق املتوسط بمنظمة الصحة العاملية. وهى منرب لتقديم السياسات واملبادرات اجلديدة يف الصحة العامة ...... اجلمهورية العربية السورية جيبويت السودان الصومال العراق عُ ام ن فلسطني قطر الكويت لبنان مرص املغرب واخلدمات الصحية والرتويج هلا، ولتبادل اآلراء واملفاهيم واملعطيات الوبائية ونتائج األبحاث وغري ذلك من املعلومات، وخاصة ما يتعلق منها بإقليم رشق اململكة العربية السعودية . اليمن املتوسط. وهى موجهة إىل كل أعضاء املهن الصحية، والكليات الطبية وسائر املعاهد التعليمية، وكذا املنظامت غري احلكومية املعنية، واملراكز املتعاونة مع منظمة الصحة العاملية واألفراد املهتمني بالصحة ىف اإلقليم وخارجه. Membres du Comité régional de l’OMS pour la Méditerranée orientale La Revue de Santé de la Méditerranée Orientale Afghanistan . Arabie saoudite . Bahreïn . Djibouti . Égypte . Émirats arabes unis . République islamique d’Iran EST une revue de santé officielle publiée par le Bureau régional de l’Organisation mondiale de la Santé pour la Méditerranée orientale. Elle Iraq . Libye . Jordanie . Koweït . Liban . Maroc . Oman . Pakistan . Palestine . Qatar . République arabe syrienne offre une tribune pour la présentation et la promotion de nouvelles politiques et initiatives dans le domaine de la santé publique et des Somalie . Soudan . Tunisie . Yémen services de santé ainsi qu’à l’échange d’idées, de concepts, de données épidémiologiques, de résultats de recherches et d’autres informations, se rapportant plus particulièrement à la Région de la Méditerranée orientale. Elle s’adresse à tous les professionnels de la santé, aux membres des instituts médicaux et autres instituts de formation médico-sanitaire, aux ONG, Centres collaborateurs de l’OMS et personnes concernés au sein et hors de la Région.

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Cover photo: © WHO / Budi Chandra

Cover 26-7.indd 4,6 23/07/2020 01:02 Vol. 26.11 – 2020

Editorial Tackling diabetes: how nurses can make the difference Hicham El Berri, F Gulin Gedik, Jamal Belkhadir, Howard Catton, Asmus Hammerich, Arwa Oweis and Slim Slama ...... 1318 Commentary Tobacco industry commissioned reports on illicit tobacco trade in the Eastern Mediterranean Region: how accurate are they? Erin Sandberg, Allen WA Gallagher and Raouf Alebshehy...... 1320 Research articles Health information systems in Jordan and Palestine: the need for health informatics training Hussein Jabareen, Yousef Khader and Adel Taweel...... 1323 Barriers to initiation of insulin therapy in poorly controlled type 2 diabetes based on self-determination theory Armin Rajab, Pegah Khaloo, Soghra Rabizadeh, Hamid Alemi, Salome Salehi, Reza Majdzadeh, Hossein Mirmiranpour, Assadollah Rajab, Alireza Esteghamati and Manouchehr Nakhjavani...... 1331 Prevalence of non-reporting of hospital medical errors in the Islamic Republic of Iran Mehrdad Askarian, Seyyed M. Sherafat, Maryam Ghodsi, Zahra Shayan, Charles Palenik, Nahid Hatam and Yavor Enchev...... 1339 Assessment of nurses’ patient safety culture in 30 primary health-care centres in Tunisia Mohamed Ayoub Tlili, Wiem Aouicha, Mohamed Ben Dhiab and Manel Mallouli...... 1347 Travel burden and geographic access to health care among children with cancer in Saudi Arabia Abdulrahman Alsultan, Abdullah Aljefri, Mouhab Ayas, Musa Alharbi, Nawaf Alkhayat, Faisal Al-Anzi, Fawwaz Yassin, Fawaz Alkasim, Qasim Alharbi, Shaker Abdullah, Mohammed Burhan Abrar and Wasil Jastaniah...... 1355 Prevalence of refractive error and visual impairment among school-age children of Hargesia, Somaliland, Somalia Zahra Abdi Ahmed, Saif Hassan Alrasheed and Waleed Alghamdi...... 1362 Risk factors associated with worse outcomes in COVID-19: a retrospective study in Saudi Arabia Anas Khan, Saqer Althunayyan, Yousef Alsofayan, Raied Alotaibi, Abdullah Mubarak, Mohammed Arafat, Abdullah Assiri and Hani Jokhdar...... 1371 Quality utilization of antenatal care and low birth weight: evidence from 18 demographic health surveys Saverio Bellizzi and Susanna Padrini...... 1381 Macromineral enrichment of white bread reduces postprandial glycaemia without altering sensory properties: a crossover study Rania El Khoury, Noor El Solh, Ammar Olabi, Imad Toufeili, Sani Hlais and Omar Obeid...... 1388 Reviews Rationing access to total hip and total knee replacement in the Islamic Republic of Iran to reduce unnecessary costs: policy brief Mohammad Soleimani, Shoresh Barkhordari, Farhad Mardani, Nasrin Shaarbafchizadeh and Fatemeh Naghavi-Al-Hosseini...... 1396 Application of geographic information systems in maternal health: a scoping review Leila Ahmadian, Fatemeh Salehi and Kambiz Bahaadinbeigy...... 1403

Eastern Mediterranean La Revue de Santé de la Health Journal Méditerranée orientale Short research communications Reproductive and behavioural risk factors of low birthweight among newborns in Al Thawra Hospital, Sana’a, Yemen Idayu Idris, Manal Sheryan, Qistina Ghazali and Azmawati Nawi...... 1415 Barriers to the use of dental services by children in Lebanon and association with parental perception of oral health care Ingrid Karam, Miran A. Jaffa and Joseph Ghafari...... 1420 Report Profil épidémiologique d’une intoxication au méthanol, El Hajeb (Maroc) Sanah Essayagh, Mariama Bahalou, Meriem Essayagh et Touria Essayagh...... 1425 WHO events addressing public health priorities Enteric and diarrhoeal diseases surveillance, prevention and control in the Eastern Mediterranean Region ...... 1430 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, Metry Al Ashkar, John Badawi, Ahmed Magdy, Amin El Sayed, Gehane Al Garraya

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. 11 – 2020

Tackling diabetes: how nurses can make the difference Hicham El Berri,1 F Gulin Gedik,2 Jamal Belkhadir,3 Howard Catton,4 Asmus Hammerich,5 Arwa Oweis 6 and Slim Slama 7

1Medical Officer for NCD Management, Department for UHC/Noncommunicable Diseases and Mental Health, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt.2 Coordinator, Health Workforce Development, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. 3Regional Chair, International Diabetes Federation Middle East and North Africa, Rabat, Morocco. 4Chief Executive Officer, International Council of Nurses, Geneva, Switzerland.5 Director, Department for UHC/Noncommunicable Diseases and Mental Health, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. 6Regional Advisor, Nursing and Midwifery, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. 7Regional Advisor for Noncommunicable Diseases Prevention, Department for UHC/Noncommunicable Diseases and Mental Health, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt. (Correspondence to: Hicham El Berri: [email protected]).

Citation: El Berri H; Gedik FG; Belkhadir J; Catton H; Hammerich A; Oweis A; et al. Tackling diabetes: how nurses can make the difference. East Mediterr Health J. 2020;26(11):1318–1319. https://doi.org/10.26719/2020.26.11.1318 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).

This year, World Diabetes Day on 14 November coincides to services, which implies the need for interventions to with the International Year of the Nurse and the Midwife, maximize their functions and performance in addressing and therefore focuses on highlighting the role of nurses the 5.9 million of shortage of nurses, 17% of which is in the prevention and management of diabetes. in the Region (9). Health workers, at primary care level, Diabetes is recognized as an important cause of play an important role in prevention and management premature death and disability globally and in the of non-communicable diseases including diabetes. Eastern Mediterranean Region, where its prevalence Nurses, as the largest group of health-care providers and has been steadily increasing since 1990, (1). Although the point of first contact, should take a leading role in the annual decline of the risk of dying from a major diabetes detection, treatment and rehabilitation, as well noncommunicable disease between the ages of 30 and as supporting health promotion and prevention efforts 70 years is slowing globally, diabetes is showing a 5% to people living with diabetes, thus allowing them to increase in attributed premature mortality (1). In 2016, participate in the decision-making regarding diabetes diabetes was the direct cause of 1.6 million deaths globally care. and 43% of all deaths before the age of 70 years occur due While recognizing that adequate numbers of well- to high blood glucose (2). Overweight and obesity are the educated nurses are key to maintaining essential strongest risk factors for type 2 diabetes (3,4). In addition, health services to effectively address the rise in diabetes increases the risk of heart disease and stroke and noncommunicable diseases including diabetes, the need is a leading cause of blindness, lower limb amputation for strengthening the nursing workforce in the Region and kidney failure. A study conducted in 35 countries remains as a challenge. Increases in numbers have not indicated that people living with diabetes are more likely been sufficient to match population growth; moreover, to experience catastrophic health expenditures with there has even been a decline in nursing numbers in an estimated increase of 4% between diabetic and non- almost half of countries in the Region since 2010 (10,11), diabetic individuals, regardless of their insurance status affecting nurses’ ability to perform in their full capacity (5). and scope of practice. Diabetes care should also be The Eastern Mediterranean Region has the highest reviewed in nursing training and updated in accordance rates of diabetes worldwide with more than 43 million with recent developments. Furthermore, nursing people living with the disease (1). Many countries leadership in policy and advocacy is imperative to change in the Region are struggling to meet the health-care practice and expand nursing capacity to address diabetes needs of people with chronic diseases. Diabetes and in the Eastern Mediterranean Region (12). It is essential its complications are a great economic challenge in that nurses take on this leadership role in a more assertive advancing universal health coverage. Several obstacles way, working with decision-makers to achieve positive exist in terms of organization of health and care systems health outcomes and provide an effective quality of care to prevent and manage diabetes, including insufficient at a lower cost (13). public investment, shortage of health workers, lack The nursing contribution to the health system is of availability and accessibility of medicines, and illustrated by six key features to prevent and manage insufficient information for decision-making (6). In diabetes as follows (14): 1) Care coordination to ensure addition, the COVID-19 pandemic has taught us how that the patient’s health needs are met over time; 2) Being vulnerable our systems are in terms of preparedness and part of a multidisciplinary approach to care based on an imposed challenges to the provision of care for patients integrated relationship between health professionals, with diabetes (7,8). allowing different practitioners to seamlessly work Health workforce shortages in the Region have a as a team to improve the quality of care; 3) mobilizing significant impact on the availability and accessibility and empowering the nursing workforce to specialize in

1318 Editorial EMHJ – Vol. 26 No. 11 – 2020 noncommunicable diseases to improve cost-effective in terms of quantity, quality and relevance to roles and sustainable treatments; 4) improving access to care; and scopes of practice to maximize the utilization of 5) empowering individuals and the community; and 6) their capacities, including diabetes care. Investment is harnessing technology to maintain access to essential also critical in creating jobs that will enable nurses to health services and reduce exposure to COVID-19. work across the full scope of practice in primary care, Such a situation has led Member States to call inpatient care settings and leadership roles where they for accelerated action to strengthen nursing in the can be available and actively involved in diabetes care (7). Region (15). The call for action highlights the need for Investing in health workforce should be part of ‘Step 0’ in investment in health workforce that impacts not only health system recovery (16). Social Development Goal 3 (SDG3) but also the other Overall, governments, health-care providers, civil SDGs on eradicating poverty, inclusive and equitable society and individuals have a shared responsibility in education, gender equality through the employment raising public awareness about the threat of diabetes, its and empowerment of women, and promoting decent prevention and management, as well as strengthening work and sustainable and inclusive economic growth. nursing and ensuring access to acceptable standards of Investments can target scaling up nursing education health care for all people living with diabetes.

References 1. World Health Organization. World Health Statistics 2020: Monitoring health for the SDGs. Geneva: World Health Organization; 2020 (https://www.who.int/gho/publications/world_health_statistics/2020/en/). 2. World Health Organization. Global report on diabetes. Geneva: World Health Organization; 2016 (https://apps.who.int/iris/bitstream/handle/10665/204871/9789241565257_eng.pdf?sequence=1). 3. Wu Y, Ding Y, Tanaka Y, Zhang W. Risk factors contributing to type 2 diabetes and recent advances in the treatment and prevention. Int J Med Sci. 2014;11(11):1185–1200. doi: 10.7150/ijms.10001 (https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4166864/). 4. Bhupathiraju SN, Hu FB. Epidemiology of obesity and diabetes and their cardiovascular complications. Circ Res. 2016 May 27;118(11):1723–1735. doi: 10.1161/CIRCRESAHA.115.306825. (https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4887150/). 5. Smith-Spangler CM, Bhattacharya J, Goldhaber-Fiebert JD. Diabetes, its treatment, and catastrophic medical spending in 35 developing countries. Diabetes Care. 2012 Feb;35(2):319-26. doi: 10.2337/dc11-1770. Epub 2012 Jan 11. PMID: 22238276; PMCID: PMC3263916. 6. Beran D. The impact of health systems on diabetes care in low and lower middle income countries. Current Diabetes Reports 2015;15(4):591 doi: 10.1007/s11892-015-0591-8. (https://www.researchgate.net/publication/272835492_The_Impact_of_Health_Sys- tems_on_Diabetes_Care_in_Low_and_Lower_Middle_Income_Countries/citation/download). 7. World Health Organization Regional Office for the Eastern Mediterranean. Rapid assessment of service delivery for NCDs during COVID-19. Cairo: WHO/EMRO; 2020 (http://www.emro.who.int/noncommunicable-diseases/publications/rapid-assessment-of-service-delivery-for-ncds-during-covid-19.html?ver=2). 8. World Health Organization. Pulse survey on continuity of essential health services during the COVID-19 pandemic. Geneva: World Health Organization; 2020 (https://www.who.int/publications/i/item/WHO-2019-nCoV-EHS_continuity-survey-2020.1). 9. World Health Organization. State of the world’s nursing 2020: investing in education, jobs and leadership. Geneva: World Health Organization; 2020. 10. FG Gedik, Buchan J, Mirza Z, Rashidian A, Siddiqi S, Dussault G. The need for research evidence to meet health workforce challenges in the Eastern Mediterranean Region. East Mediterr Health J. 2018.24.9.811–812. https://doi.org/10.26719.2018.24.9.811 11. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Strengthening the nursing workforce to advance universal health coverage in the Eastern Mediterranean Region, EM/RC66/R.3. 2019. Cairo: WHO/EMRO; 2019 (https://applications.emro.who.int/docs/RC66-R3-eng.pdf?ua=1). 12. Affara FA, Tuipulotu AA, Al Darazi FA, Aiken LH, Betker C, Buchan J, et al. Nurses: a voice to lead nursing the world to health. Ge- neva: International Council of Nurses; 2020 (https://2020.icnvoicetolead.com/wp-content/uploads/2020/03/IND_Toolkit_120320. pdf). 13. Peimano M, Tabatabaei O, Paajouhi M. Nurses’ role in diabetes care: a review. Iran J Diabetes Lipid Dis. 2010;9(4):1-9 (https:// www.researchgate.net/publication/236985435_Nurses’_Role_in_Diabetes_Care_A_review). 14. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). The nurse and diabetes: Report by the International Council of Nurses for World Diabetes Day 2020. Cairo: WHO/EMRO; 2020 (https://applications.emro.who.int/docs/ RC_Technial_Papers_2019_4_en.pdf?ua=1). 15. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Strengthening the nursing workforce to advance universal health coverage in the Eastern Mediterranean Region, EM/RC66/R.3. Cairo: WHO/EMRO; 2019 (https://applications.emro.who.int/docs/RC66-R3-eng.pdf?ua=1, accessed on 22 October 2020). 16. World Health Organization. UHC 2030. Living with COVID-19: Time to get our act together on health emergencies and UHC. Discussion paper, published 27 May 2020. (https://extranet.who.int/sph/sites/default/files/document-library/document/ UHC2030%20Discussion%20paper%20on%20health%20emergencies%20and%20UHC%20-%20May%202020.pdf, accessed on 27 October 2020).

1319 Commentary EMHJ – Vol. 26 No. 11 – 2020

Tobacco industry commissioned reports on illicit tobacco trade in the Eastern Mediterranean Region: how accurate are they?

Erin Sandberg,1 Allen WA Gallagher2 and Raouf Alebshehy2

1Vital Strategies, New York, United States of America. 2University of Bath, Bath, United Kingdom. (Correspondence to: Raouf Alebshehy: r.alebshehy@ exposetobacco.org) Citation: Sandberg E; Gallagher AWA; Alebshehy R. Tobacco industry commissioned reports on illicit tobacco trade in the Eastern Mediterranean Region: how accurate are they? East Mediterr Health J. 2020;26(11):1320–1322. https://doi.org/10.26719/emhj.20.131 Received: 28/07/20; accepted: 07/10/20 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)

Tobacco industry-commissioned reports on the illic- occurring in the Eastern Mediterranean Region with a it tobacco trade are one of the few data sources on the recent Oxford Economics report (6) providing estimates practice across Europe and Asia. The tobacco industry of illicit trade in Egypt, Jordan and Lebanon. is now funding estimates of illicit trade in a number of Tobacco companies have an incentive to misrepresent countries in the World Health Organization (WHO) East- the size of the illicit tobacco trade, resulting in industry- ern Mediterranean Region, specifically Egypt, Jordan and funded research having been widely criticized for Lebanon. These estimates come from a recent report by its unreliability and exaggeration of the scale of the Oxford Economics, which was funded by major trans- illicit market (7). Tobacco companies regularly cite national tobacco companies. Industry-funded studies of industry-funded reports about the illicit trade [yet fail to the illicit tobacco trade have been found to consistently acknowledge the funding link, as seen in a recent Philip fail to meet the standards of quality and transparency ex- Morris International (PMI) interview (8)] as part of their pected of peer-reviewed research. Moreover, the scale of efforts to oppose public health policy (9). As such, we have the problem would appear exaggerated in order to aid the scrutinised the new Oxford Economics report to establish industry’s efforts to oppose tobacco controls by arguing the reliability of its estimates of illicit trade. that such measures would actually increase illicit trade. In March 2020, global forecasting company Oxford A critical look at this new report suggests that this trend Economics (10) released a report titled “Levant Illicit continues, while concerns remain over the reliability of Tobacco 2019” (6), commissioned by British American the data and estimates claimed, stressing the need for in- Tobacco (BAT), Japan Tobacco International (JTI) and dependent research of the illicit tobacco trade in the East- Philip Morris SA (a subsidiary of PMI). It examines the ern Mediterranean Region. illicit cigarette market in Egypt, Jordan and Lebanon. While countries in the Eastern Mediterranean The report, which is a business document and not peer- Region are seeing progress in the implementation of reviewed academic research, is concerning for several WHO MPOWER measures (1), WHO reports on smoking reasons. prevalence in the Region indicate it will not achieve its As per the report’s disclaimer, it was prepared “in 30% relative prevalence reduction target (12.6%) by the accordance with specific terms of reference” agreed by year 2025 (2). Decreasing the affordability of cigarettes Oxford Economics and the tobacco companies. These is recognized as the most effective means to reduce terms of reference are not disclosed and may have prevalence and help the Region achieve its target, but a influenced how the report portrays the tobacco industry major obstacle to this is the illicit tobacco trade, which and its involvement in the illicit market. increases accessibility and affordability of tobacco Also of concern is Oxford Economics’ existing tobacco products. The practice has been a problem for a number industry ties, including a working relationship with of countries in the Region for decades, driven in large part PMI dating back to 2017 when PMI announced that by transnational tobacco companies having smuggled Oxford Economics would receive funding from its PMI their own product into countries, including Jordan and IMPACT initiative (11,12). Past Oxford Economics reports Lebanon, from as early as the mid-1970s (3,4). However, on illicit trade have been criticised by academics and the scale of the Region’s current illicit tobacco trade is nongovernmental organizations (NGOs) for their reliance difficult to measure due to its illegality as well as data on the industry for their data, for the methods of analysis collection and analysis complexities. Transparent public used, and for the presentation of the reports appearing to data on the topic of illicit tobacco trade is limited, and in mislead readers (13,14). Most recently, Oxford Economics’ many countries it is non-existent (5). “Asia Illicit Tobacco Indicator 2017” report was critiqued It is within this context that the tobacco industry in a report by the Southeast Asia Tobacco Control Alliance has become a major funder of data on illicit trade, often (15). by commissioning reports that provide estimates of Many of the concerns raised over previous Oxford illicit trade in a geographical area. This practice is now Economics reports hold true in the new report on the

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Levant region. The choice of featured markets in the those countries were captured, thus skewing the final report is questionable and no justification is given in the figures. report for the selection of countries mentioned. Despite Concerns over the accuracy of the report’s estimations the report’s title referring to the Levant region, only three extend to the report’s recommendations, as well. The countries within this geographical area are featured in policy recommendations come from the Transnational the analysis and no justification is provided for why other Alliance to Combat Illicit Trade (TRACIT), an NGO with countries were left out. Since Egypt, Jordan and Lebanon extensive tobacco industry ties. Among other links to the have all experienced tax increases in recent years, these industry, TRACIT has previously listed BAT, JTI and PMI countries may have been chosen to help illustrate the as members on its website, with its current website still industry narrative that increased taxes lead to increased citing PMI as a member (16); however, none of TRACIT’s illicit tobacco trade. partnerships with tobacco companies were mentioned in As with previous industry-commissioned reports on the report. illicit tobacco trade (7), the primary data input for this One of the report’s recommendations is to “rationalize report was highly susceptible to industry interference. tax policy”, which supports the tobacco industry’s efforts To estimate levels of illicit tobacco trade, the report relies to create a link between increased cigarette taxes and on empty pack surveys, where discarded cigarette packs purported growth in illicit tobacco trade. Evidence are collected and then tested by tobacco companies to indicates16 that this depiction of the relationship between identify if the product is from their own supply chain. tax and illicit trade is over-simplified as countries with Allowing tobacco companies to determine this opens low cigarette taxes and prices often have larger illicit the data up to manipulation, since tobacco companies cigarette markets than countries with higher taxes and have a vested interest in under-reporting their own prices (17). product on the illicit market. The report fails to disclose Therefore, the report, data and estimates would appear the known limitations of such surveys and does not unreliable and highlights the urgent need for independent provide sufficient detail for surveys to be replicated by research on the illicit tobacco trade. With no comparable, independent researchers to validate the findings. independent alternatives, Oxford Economics reports are one of the only major sources of data on the illicit trade The report does acknowledge one flaw, albeit solely across Asia, and now the Eastern Mediterranean Region. via a footnote on page 7. The authors indicate that only More independent data are needed to provide accurate exports from the three featured countries to those same insight into the illicit tobacco trade and to verify findings three countries are included in the analysis. This is in industry-funded reports. problematic, as leaving out products that were legally exported from the three countries to other countries not Funding: All authors acknowledge the support of featured in the report ultimately lowers the estimated Bloomberg Philanthropies Stopping Tobacco Organiza- total legal consumption of the three featured countries. tions and Products project funding (www.bloomberg. This, in turn, makes the percentage of illicit cigarettes in org). the three countries larger than if all legal exports from Competing interests: None declared.

References 1. Heydair G, Zaatari G, Al-Lawati J, El-Awa F, Fouad H. MPOWER, needs and challenges: trends in the implementation of the WHO FCTC in the Eastern Mediterranean Region. East Mediterr Health J. 2018;24(1):63–71. https://doi.org/10.26719/2018.24.1.63 2. El-Awa F, Bettcher D, Al-Lawati JA, Alebshehy R, Gouda H, Fraser CP. The status of tobacco control in the Eastern Mediterrane- an Region: progress in the implementation of the MPOWER measures. East Mediterr Health J. 2020;26(1):102–109. https://doi. org/10.26719/2020.26.1.102 3. World Health Organization Regional Office of the Eastern Mediterranean (WHO/EMRO). The cigarette “transit” road to the Islamic Republic of Iran and Iraq: illicit tobacco trade in the Middle East. Cairo: WHO/EMRO; 2008 (https://applications.emro. who.int/dsaf/dsa908.pdf, accessed 24 July 2020). 4. Tobacco Control Research Group. Eastern Mediterranean Region. In. TobaccoTactics.org: University of Bath (https://tobaccotactics.org/wiki/eastern-mediterranean-region/) (last edited 30 April 2020). 5. Prasad V, Schwerdtfeger U, El-Awa F, Bettcher D, da Costa e Silva V. Closing the door on illicit tobacco trade, opens the way to better tobacco control. East Mediterr Health J. 2015;Sep 8;21(6):379-80. https://doi.org/10.26719/2015.21.6.379. 6. Oxford Economics. Levant Illicit Tobacco 2019. (https://www.oxfordeconomics.com/recentreleases/levant-illicit-tobacco-2019. Published 2020, accessed 24 July 2020). 7. Gallagher AWA, Evans-Reeves KA, Hatchard JL, Gilmore AB. Tobacco industry data on illicit tobacco trade: a systematic review of existing assessments. Tob Control. 2018: tobaccocontrol-2018-054295. 8. Philip Morris International. Philip Morris International’s Taylan Suer discusses IQOS and local market response. Executive, 8 May 2020 (https://www.executive-magazine.com/brand-voice/philipmorris-internationals-taylan-suer-discusses-iqos-and-lo-� cal-market-response, accessed 24 July 2020).

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9. Ulucanlar S, Fooks GJ, Gilmore AB. The Policy Dystopia Model: an interpretive analysis of tobacco industry political activity. PLoS Med. 2016;13(9):e1002125. 10. Tobacco Control Research Group. Oxford Economics. In. TobaccoTactics.org: University of Bath. (https://tobaccotactics.org/wiki/ oxford-economics). (Last edited 9 August 2017). 11. Tobacco Control Research Group. PMI IMPACT. In. TobaccoTactics.org: University of Bath. (https://tobaccotactics.org/wiki/ pmi-impact). (Last edited 26 October 2017). 12. Tobacco Control Research Group. List of successful PMI IMPACT Applicants. In. TobaccoTactics.org: University of Bath. (https:// tobaccotactics.org/wiki/list-of-successful-pmi-impact-applicants). (Last edited 21 March 2019). 13. South East Asia Tobacco Control Alliance (SEATCA). Failed: a critique of the ITIC/OE Asia-14 Illicit Tobacco Indicator 2013. Bang- kok: SEATCA; 2015 (https://seatca.org/dmdocuments/Asia%2014%20Critique_Final_20May2015.pdf; accessed 7 November 2017). 14. South East Asia Tobacco Control Alliance (SEATCA). Illicit tobacco indicator 2012: more myth than fact. A critique by SEATCA. Bangkok: SEATCA; 2013 (http://seatca.org/dmdocuments/ITIC%20report_More%20Myth%20than%20Fact_2%20July %202014.pdf, accessed 1 October 2014). 15. South East Asian Tobacco Control Alliance (SEATCA). Still defective: Asia illicit tobacco indicator 2017 report. Bangkok: 2020 (https://stoptobacco.sharepoint.com/sites/STOPBriefingonTrackingTracing/Shared%20Docu ments/General/Still%20Defec- tive-Asia%20Illicit%20Tobacco%20Indicator_June%202020.pdf, accessed 24 July 2020). 16. Tobacco Control Research Group. Transnational Alliance to Combat Illicit Trade (TRACIT). University of Bath. (https://tobaccotactics.org/wiki/tracit). (Last edited 11 June 2020). 17. World Bank Group. Confronting illicit tobacco trade: a global review of country experiences. Washington DC: World Bank Group; 2019 (http://documents.worldbank.org/curated/en/677451548260528135/pdf/133959-REPLPUBLIC-6-2-2019-19-59-24-WB-� GTobaccoIllicitTradeFINALvweb.pdf, accessed 28 May 2019).

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Health information systems in Jordan and Palestine: the need for health informatics training

Hussein Jabareen,1 Yousef Khader2 and Adel Taweel3

1College of Nursing, Hebron University, Hebron, Palestine (Correspondence to: Hussein Jabareen: [email protected]). 2Department of Public Health, Jordan University of Science and Technology, Irbid, Jordan. 3Department of Computer Science, Birzeit University, Ramallah, Palestine.

Abstract Background: Some Arab countries have health information systems (HIS) in place but they lack well trained IT staff. Poor management and lack of appreciation of the importance of HIS are major barriers to development and adoption of HIS in Arab hospitals. Aims: This research is part of a survey carried out to determine health informatics (HI) use and to assess the training needs of health professionals in Jordan and Palestine. Methods: A survey was conducted in 2017 among employees in all health professions at 14 hospitals in Jordan and Pales- tine to assess their use of the HI system and to assess the HI skills needed in both countries. Results: The majority of respondents reported that their hospital departments were employing computer systems to run services. More than half had received training in computer skills but also half said they needed specialized training in HI. Between 58.0% and 73.6% agreed that their hospitals provided the necessary support to operate HI systems. The vast majority (86.0%) of health professionals reported that they needed skills to monitor diagnosis and treatment, including access to clinical findings. Other skills needed included using shared hospital services (85.6%), using medical records (84.7%), managing electronic patient data (84.5%), using patient medical records to conduct clinical research (83.4%), and using tele-care services and technologies effectively (75.9%). Conclusions: Health professionals in Palestine and Jordan are in need of training in HI and therefore educational programmes in the area of HI are strongly recommended. Keywords: health information systems, health informatics, health professionals, Jordan, Palestine Citation: Jabareen H; Khader Y; Taweel A. Health information systems in Jordan and Palestine: the need for health informatics training. East Mediterr Health J. 2020;26(11):1323–1330. https://doi.org/10.26719/emhj.20.036 Received: 22/05/19; accepted: 16/12/19 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 Arab and Western countries in the information systems available (and used) (8–10). However, it seems that both Using computer and health informatics is critically groups of countries are facing similar challenges in the important in improving the quality of the health care enforcement of HISs (11). For instance, in an international system, patient care and health outcomes (1). Health in- comparison of factors inhibiting physicians’ use of HIS formation systems (HIS) or health informatics (HI) is a in the United States, Chile and Germany, Gewald et al. multidisciplinary domain that utilizes health informa- found that each country developed its own HIS but took a tion technology (HIT) to enhance health care services via unique approach to fostering the implementation of IT in any combination of higher efficiency, higher quality and their health care settings and applied it differently at each new opportunities. The HIS is information design and management level (12). They reported that leadership build applied to the field of health care, essentially “the and management structures had a significant role in management and utilization of patient health care infor- the Western health care services in fostering the use of mation” (2). Electronic health systems are being used by IT allied with the user, system, and process obstacles. health professionals to implement daily care manage- Similarly, each Arab country had a unique culture and ment, avoid complications, prevent medical and medica- approach to health services, so HIS had to be specific and tion errors, and carry out clinical research (3,4). Electronic appropriate and in keeping with specific health policies health systems make the management of patient records (13). In many health care institutions, data are collected easier and safer while HI supports health professionals, manually on paper rather than by digital data entry, but consumers, patients and other stakeholders in their deci- still the collected data are not complete, which results in sion-making to achieve desired outcomes. This support is a burden for patient monitoring as well as data analysis. accomplished through the use of information structures, In addition, regulations regarding the ethical use of information processes and information technology (5,6). clinical data are not adequate in many Arab countries (14). Most of the Arab countries are lagging behind in It is essential that health policy experts, researchers and using an HIS due to lack of financial resources and other professionals create systems and policies that are staff competencies (7). There is a huge gap between the comprehensive and improve health care services (15).

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Some Arab countries have an HIS in place but they and industrial expertise in both computing and health to lack well trained IT staff, data collectors, data entry develop innovative, integrated HI curricula. The HiCure personnel and data analysts (7). Poor management and project develops HI as integrated pathways within bureaucracy as well as a lack of appreciation of the the undergraduate degrees of both the information importance of HIS are major barriers to the development technology and health-oriented programmes in Palestine and adoption in Arab hospitals (16). Cost was an obstacle and Jordan. The development of HI skills integrated to HIS development in many Arab countries, but it was within the existing degrees will ensure graduate students less of a concern in Saudi Arabia compared with others with competent skills founded on a solid grounding (16). The shortage, however, of competent IT staff was an within their educational background. In addition to obstacle in Syria and Saudi Arabia. Some efforts are under meeting their intended educational learning outcomes, way to address these shortcomings, but more financial HI skills will also become an essential part of students’ resources need to be allocated to further develop IT profession employed as mechanisms that will improve human resources and an HIS that fit local needs. the quality of health care by graduates qualified in both In many Arab countries, poor funding is the main health and computing, and advance the health domain obstacle to implementing the HIS, while in countries towards information-driven, efficient and effective of the Gulf Cooperation Council, economic funds are evidence-based practice (23,24). available but the main barriers were the lack of qualified Implementation of HIS is complex and relies on personnel, the lack of engagement of clinical staff in organizational, structural, technological and human utilizing HIS, and ethical and privacy concerns (17,18). factors to be complementary and successful (25). Assessing According to Alsadan et al., Saudi Arabia and the United the impact of a complex HIS from the perspective of Arab Emirates were the most advanced Arab countries users is considered one of the most efficient evaluation in utilizing an HIS (7), the authors recommended that methods in comparison with other methods (26). Although cooperation and exchange of experiences between the use of HIS has pervaded health care settings in the different Arab countries is needed to overcome some of Arab world and worldwide, methodologies to evaluate the common barriers in implementing HIS. its impact in these settings have not developed with the Hayajneh and Zaghloul recommended that medical same momentum (4). So, our study aimed to assess the and health curricula should be revised to include and use of HIS by health professionals and assess the needed integrate HIS and that new programmes in HI should HI skills in Palestine and Jordan. be established (16). Similar findings were reported by Shaban et al. in 2010 in their study on trauma registry Methods in the United Arab Emirates, where the lack of funding and resources, the lack of qualified personnel in HI and A descriptive cross-sectional design was conducted the need for user friendly software for data entry were among employees of all health professions at 14 govern- the main barriers (19). In developed countries such as the mental, nongovernmental, and private hospitals in Jor- United States, despite its advancement in HI, barriers dan and Palestine. A sample of health professionals was to using electronic health records as revealed by studies selected from those who were working in these hospitals conducted over 10 years earlier were mainly costs and during the period March–June 2017. Within each hospi- technical and communication difficulties (20). Academic tal, the study questionnaire was randomly administered institutions in the Arab world successfully provide to 20% of the total number of employees. national and international health institutions with This study is part of a survey that was carried qualified health care professionals, including medical out to determine HI usage and to assess the training doctors, pharmacists and nurses, while HI remains a needs of health professionals in Jordan and Palestine. newer field. With the recent realization and emphasis on Two methods of sampling were adopted to satisfy the the need for HI, some universities in the Arab countries declared objectives of the study. The first method was a have started providing a few courses, tracks or degrees purposeful (convenience) sampling technique which was in HI. In Egypt, Jordan and Palestine a few universities used to access targeted hospitals. Letters, questionnaire, provide HI training and courses for undergraduate and information sheets about the study were sent to students in the health and IT fields. In Saudi Arabia the ministries of health responsible for governmental and the United Arab Emirates, some universities offer hospitals and to the administrations of nongovernmental advanced degrees in HI. The current situation in the hospitals asking their permission to allow the research Arab world requires further development of academic team to distribute the questionnaire and collect data programmes that can meet the needs of health care from health professions employees. All 14 hospitals we providers (15,21). approached agreed to participate in this study. The second In Palestine and Jordan, HIS has recently been sampling procedure was within each hospital, where the implemented in some areas but with various challenges research team targeted the available employees who were and obstacles, and its application is still limited to on duty during data collection shift. The data collection electronic patient records (22). HiCure is an Erasmus + process was facilitated by permissions granted from funded project. The project has a well-placed the Jordanian and Palestinian ministries of health and international consortium that combines strong academic the administrations of the nongovernmental hospitals.

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This facilitated entering these hospitals during different 11% in private hospitals. The survey covered all health working shifts to reach as many diverse employees as units in hospitals. About 74% of respondents were work- possible and include opinions of all health professionals. ing in the major medical, surgical, allied health and high Participants were recruited from 3 working shifts (day, dependency departments (Table 1). However, 5% stated evening, night) from each hospital during the data they were working in other departments not listed in the collection phase. Data collection started with the available questionnaire. health employees in the different departments in the day shift. After that, the research team revisited the hospitals Years of experience during the evening and night shifts. The median years of experience in the profession was 5 The questionnaire sought information about (range 1–35) years. While the median experience in using demographic characteristics of participants, use of computer systems was 4 (range 0–30) years. The medi- computerized health systems, organizational support for an duration of using HIS was 2 (range 0–23) years. The HI, training and usage of HI, and the needed HI skills. majority of professionals in Palestinian and Jordanian The perception of employees regarding the importance hospitals started recently to use health computerized and adequacy of HI for health care practice at their systems, and more than one-fifth did not have any expe- institutions was explored by asking 10 questions using rience with HI (Table 2). a 5-point Likert-type scale. The questionnaire was self- Computer use in institutions completed, filled out within the hospital setting during the break time in a place that was convenient to each At the institutional level, more than 67% of respondents participant. Completing the questionnaire took on reported that their hospital departments were employ- average 10 minutes. ing computer systems to run their services, especially in financial management (77%), medical laboratory (74%), Ethical approval was obtained from the Institutional pharmacy (71%), electronic records (67%), and top man- Review Board at Jordan University of Science and agement (66%) (Table 3).The use of computer systems Technology. was reported to a lesser extent for electronic prescrip- Data were analysed using SPSS, version 20. Data were tions (59%) and managing medical devices (50%). described using means, medians, and percentages as appropriate. Use of computer by physicians, allied health professionals, and nurses Results When the analysis was limited to physicians, allied health professionals and nurses, 84.9% in Palestine and Participants 68.8% in Jordan reported that they used computers to A total of 579 health employees from 14 hospitals re- carry out their duties (Table 4). Nurses and allied health sponded to the questionnaire, a response rate of 83%. professionals in Palestine were more likely to report the About 34% of the respondents were from Jordan and 66% use of computers to accomplish their tasks. About 75.3% from Palestine. The mean age of the respondents was of health professionals in Palestine and 62.2% in Jordan 32 (range 20–65) years. About 18% had a Diploma, 71% a reported the use of electronic medical records. Nurses Bachelor’s degree and 7% a post graduate degree (High and allied health professionals in Palestine were more Diploma, Masters, PhD, or specialization in medicine). likely to report the use of electronic medical records than About 75% of the respondents were employed in govern- those in Jordan. mental hospitals, 14% in nongovernmental hospitals, and Training on computer use for health professionals Table 1 Distribution of Jordanian and Palestinian health More than half of health professionals received training professionals (n = 579) according to department/unit, 2017 on computer skills (Table 4). Almost the same proportion Department/unit % reported that they needed specialized training in HI (Ta- Medical department 25.7 ble 5). The majority of health professionals perceived that Allied health department 19.2 it is important to have HIS in their institution and about 52% of Jordanian and 60% of Palestinian health profes- Surgical department 16.2 sionals reported that their institutions had adequate HIS High dependency unit 12.8 (Table 5). Paediatrics department 4.5 Outpatient clinics 4.3 Organizational support for health informatics Administration 3.8 Most employees were satisfied with the support provid- Emergency room 3.3 ed by their organizations for the use of HI programmes Maternity department 3.1 (Table 6). For instance, about three-quarters (73.6%) reported that their institutions provided a supportive envi- Operation room 2.1 ronment for HI programmes; two-thirds (66.9%) reported Other 5.0 that their institutions had the necessary infrastructure

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Table 2 Distribution of Jordanian and Palestinian health professionals (n = 579) according to years of experience, 2017 Years of experience In health profession Using computer systems Using health information systems No. % No. % No. % 0 0 0 67 12 120 22 1–5 279 50 266 48 376 68 6–10 123 22 108 19 48 8 11–15 63 12 86 16 7 1 16–35 89 16 27 5 3 1 Total 554 100 554 100 554 100

that enables clinicians while using HI and their institu- Table 3 Use of computer systems according to department/ tions were committed to promoting and improving the unit as reported by Jordanian and Palestinian health implementation of HIT (68.3%). professionals (n = 579), 2017 Professional department/unit Computer use The needed health informatics skills % The majority of health professionals reported that they Financial management 77 were in need of HI skills (Table 7); 86.0% reported that Medical laboratory 74 they needed skills to monitor patients’ diagnosis and Pharmacy 71 treatment, including access to clinical findings. Other skills needed included using shared hospital services Electronic records 67 (85.6%), using medical records (84.7%) and managing Top management 66 electronic patient data (84.5). Electronic prescription 59 Managing medical devices 50 Discussion Logistics 44 Telemedicine in education 32 The findings of this survey have several significant theoretical and practical implications for academia, the health care sector and government. Having experience in computer systems makes it easy to learn HI systems. financial obstacles (7). In Jordan for example, the field In particular, our results show that the use of computer of HIT started only recently, thus not many allied health systems is not limited to a specific department. The ma- professionals use it. However, it has been suggested that jority of the participants were using these systems in the new health information technologies in the 21st century medical laboratory and the pharmacy to run their daily can transform the Arab world as societies need strong and transactions and operations. Electronic records and pre- efficient health policies to improve patient care (9). One scriptions were also used by almost two-thirds of the par- possible reason for not widely adopting HIT in Jordan is ticipants. Although one-third were using telemedicine, the negative perception of its importance (16). Moreover, they demonstrated a strong willingness to expand the research in the region has shown that poor funding, lack use to facilitate their daily tasks. of qualified personnel or their engagement in utilizing In comparing the 2 countries, we found that nurses HIT are the main obstacle to implementing it (17). and allied health professionals in Palestine were more There are some limitations to this study. It was carried likely to report the use of the computer to accomplish their out as part of a large survey to determine the extent of tasks. Additionally, nurses and allied health professionals usage of HIS, to assess the training needs, and to explore in Palestine were more likely to report the use of electronic the attitudes of health professionals in Jordan and medical records than those in Jordan. Nevertheless, most Palestine towards HI. So, we neither tested any hypothesis Arab countries do not use HIT very often because of nor examined associations between variables. The

Table 4 Computer use and training by Jordanian and Palestinian health professionals (n = 579), 2017 Profession Computer use Training in computer skills Jordan Palestine Jordan Palestine Physician 79.5 80.7 67.5 47.4 Nurse 56.6 84.7 50.0 63.7 Allied health professional 70.0 88.8 45.2 56.3 Overall 68.8 84.9 56.8 59.4

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Table 5 Distribution of Jordanian and Palestinian health professionals (n = 579) perceptions of the health informatics situation in their institutions, 2017 Profession There is a need for specialized Having a health information Our health information system training system is important is adequate Jordan Palestine Jordan Palestine Jordan Palestine Physicians 49.4 50.9 81.7 75.4 59.8 52.6 Nurses 71.6 64.2 86.5 88.4 46.7 60.0 Allied health professionals 61.3 48.8 87.1 81.3 45.2 66.3 Overall 60.1 58.5 84.5 84.7 52.1 60.2

sample size included 20% of health employees working in Another limitation of the analysis of this survey was the targeted 14 hospitals but these could not be described the small numbers within the subgroups. About 74% as representative of all health employees in Jordan and of our respondents were working in 4 major medical, Palestine. The survey was carried out in a stressful period surgical, allied health and high dependency departments; after the introduction of HIS in many of these hospitals, only 21% were working in the remaining 6 departments, and thus participants might not have been typical of and 5% were working in various other departments. all those in the original populations. Comparisons and Nonetheless, the survey does throw up some potentially similarities with other studies noted must therefore be important issues concerning these subgroups. treated with caution. Many studies, especially in the Arab Our results showed that more than half the health world, have reported that workloads were increased after care professionals had some training in computers skills, the introduction of HIS, and clinicians mainly complained however, large proportions among different professions about the increased paperwork and IT workload (8,16,17). in both cohorts reported needing more specialized This raises the issue of the nonrespondents as they may training in HI, suggesting a perceived lack of confidence perhaps have been the busiest professionals, those who in their current knowledge. Similarly, in an Australian could not find the time to fill out the questionnaire. study, almost half the nurses indicated a need for more In order to make it comprehensive, the questionnaire computer training to better meet their job requirements covered a wide range of topics concerning the (28). In the same study, nurses, as the largest users of training needs and impact of HI usage at individual, computer technology, considered that employers often institutional and national levels: the cost of this broad did not encourage information and computer technology scope was the inability to focus on specific clinical or training. Consistent with this, Trivedi and Joshi reported professional areas such as electronic prescribing and that more than three-quarters of health care professionals electronic triaging. Furthermore, the questionnaire in a rural medical college in India had no formal computer contained many questions about previous experience training (29). with using computers and HIS and training of health Similar to the findings of a study in hospitals in professionals and this could have produced some recall Tehran (30), we found considerable variation in computer bias. Furthermore, we did not investigate the duration of training experiences across the 3 groups of health using computers by health professionals nor the onset or professions in both settings. Physicians received more frequency of using electronic medical records. This is of training than other health care professionals in the paramount importance because sustainability is a critical Jordan cohort, while nurses received more training in factor in achieving improvements in patient health the Palestine cohort. Nurses in both countries perceived outcomes (27). a higher need for more specialized training in HI and

Table 6 Perception of institutional support for health informatics among Jordanian and Palestinian health professionals (n = 579), 2017 Institutional support for health informatics No. % The institution provides a supportive environment for health informatics programmes 425 73.6 The institution has the necessary infrastructure that enables clinicians while using health informatics 387 66.9 The institution is committed to promoting and improving the implementation of health information technology 390 68.3 My organization provides a supportive environment and/or provides the necessary training and resources for the proper use of electronic health systems 334 58.0 My organization has the necessary infrastructure, including staff and financial resources to support electronic health systems. 351 61.0 My organization promotes the use of health computing technology and/or provides sufficient encouragement for the use of electronic health systems 356 61.9

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Table 7 Key health informatics skills needed reported by Finally, and although the majority of health care health professionals in Jordan and Palestine (n = 579), 2017 professionals in both setting believed that it was Skill % important to have HI system in their institutions, Monitoring patient diagnosis and treatment 86.0 obstacles to implementing HIT still exist. To overcome Using shared hospital services 85.6 the challenges related to the use of HIT by health Using patient medical records 84.7 professionals in Jordan and Palestine, medical and health Managing electronic patient data 84.5 curricula need to be revised to include and integrate HIT, Using patient medical records for clinical research 83.4 and new programmes in HI need to be developed (16). Telemedicine and tele-care services 75.9 Indeed, some universities in Jordan and Palestine have recently started to provide HI training and courses for Using coding standards 73.8 undergraduate students in the health and IT fields. In conclusion, health professionals in Palestine computer skills than other health care professionals. and Jordan are in need for training in HI and therefore Other researchers have reported similar interest among educational programmes in the area of HI are strongly nurses towards enhancing their careers (13). recommended.

Acknowledgement This paper reflects the views only of the authors; the European Commission cannot be held responsible for any use which may be made of the information contained therein. The authors would like to thank the HiCure members who contributed to this study. Funding: This study, part of the HiCure project, has been funded with support from the European Commission. Competing interests: None declared.

Systèmes d'information sanitaire en Jordanie et en Palestine : nécessité d'une formation en informatique sanitaire Résumé Contexte : Certains pays arabes disposent de systèmes d’information sanitaire, mais ils manquent de personnel informatique bien formé. Une mauvaise gestion et un manque d'appréciation de l'importance des systèmes d'information sanitaire constituent des obstacles majeurs au développement et à l'adoption de ces systèmes dans les hôpitaux du monde arabe. Objectifs : La présente recherche fait partie d'une enquête menée pour déterminer l'utilisation de l'informatique sanitaire et pour évaluer les besoins de formation des professionnels de santé en Jordanie et en Palestine. Méthodes : En 2017, une enquête a été menée auprès des employés de toutes les professions de santé de 14 hôpitaux en Jordanie et en Palestine afin d’évaluer leur utilisation du système d’information sanitaire et de déterminer les compétences en informatique sanitaire nécessaires dans les deux pays. Résultats : La majorité des répondants ont indiqué que leurs services hospitaliers utilisaient des systèmes informatiques pour gérer leurs services. Plus de la moitié a reçu une formation en informatique, mais la moitié a également déclaré avoir besoin d'une formation spécialisée en informatique sanitaire. Entre 58,0 % et 73,6 % ont convenu que leurs hôpitaux fournissaient le soutien nécessaire au fonctionnement des systèmes d'information sanitaire. La grande majorité (86,0 %) des professionnels de santé ont déclaré avoir besoin de compétences pour surveiller le diagnostic et le traitement, y compris l'accès aux résultats cliniques. Les autres compétences nécessaires comprenaient le recours aux services hospitaliers partagés (85,6 %), l'utilisation des dossiers médicaux (84,7 %), la gestion électronique des données des patients (84,5 %), l'utilisation des dossiers médicaux des patients pour mener des recherches cliniques (83,4 %) et l'utilisation efficace des services et des technologies de télésoins (75,9 %). Conclusions : Les professionnels de santé en Palestine et en Jordanie ont besoin d'une formation en informatique sanitaire. Par conséquent, des programmes d’éducation dans ce domaine sont fortement recommandés.

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ُظم ناملعلومات الصحية يف األردن وفلسطني: احلاجة إىل التدريب يف جمال املعلوماتية الصحية حسني جبارين، يوسف خرض، عادل الطويل اخلالصة اخللفية: يوجد يف بعض البلدان العربية ُن ُظم معلومات صحية قائمة، إال أهنا تفتقر إىل العاملني َّاملدربني ًتدريبا ًجيدا يف جمال تكنولوجيا املعلومات. ِّ ل ويشكسوء اإلدارة وعدم تقدير أمهية ُنظم املعلومات الصحية عوائق رئيسية أمام تطوير ُظم ناملعلومات الصحية واعتامدها يف املستشفيات بالبلدان العربية. األهداف: ّيمثل هذا البحث ًجزءا من ٍمسح ُجري ألتحديد استخدام املعلوماتية الصحية، ولتقييم احتياجات تدريب املهنيني الصحيني يف األردن وفلسطني. طرق البحث: ُأجري مسح يف عام 2017 للعاملني يف مجيع املهن الصحية يف 14 مستشفى يف األردن وفلسطني لتقييم استخدامهم لنظم املعلومات الصحية وتقييم املهارات التي حيتاجون إليها يف جمال املعلوماتية الصحية يف كال َالبلد ْين. النتائج: أفاد غالبية املستجيبني بأن أقسام املستشفيات التي يعملون فيها تستخدم ُن ً ظامحاسوبية لتشغيل اخلدمات. وقد َّتلقى أكثر من نصفهم ًتدريبا عىل مهارات احلاسوب، ولكن نصفهم ًأيضا قالوا إهنم بحاجة إىل ٍتدريب ٍ يف متخصصجمال املعلوماتية الصحية. ووافق ما بني 58.0% و73.6% عىل أن املستشفيات التي يعملون فيها َّقدمت الدعم الالزم لتشغيل ُنظم املعلومات الصحية. وأفادت الغالبية العظمى ) %( 86.0من املهنيني الصحيني أهنم حيتاجون إىل مهارات لرصد التشخيص والعالج، بام يف ذلك إتاحة النتائج الرسيرية. وشملت املهارات األخرى الالزمة استخدام خدمات املستشفيات املشرتكة )85.6%(، واستخدام السجالت الطبية ) %(، 84.7وإدارة بيانات املرىض اإللكرتونية )84.5%(، واستخدام السجالت الطبية للمرىض إلجراء البحوث الرسيرية )83.4%(، واستخدام تكنولوجيات وخدمات الرعاية عن ُبعد بفعالية )%75.9(. االستنتاجات: حيتاج املهنيون الصحيون يف فلسطني واألردن إىل التدريب يف جمال املعلوماتية الصحية، ولذلك َيوص بشدة بتوفري برامج تعليمية يف هذا املجال.

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Barriers to initiation of insulin therapy in poorly controlled type 2 diabetes based on self-determination theory

Armin Rajab,1 Pegah Khaloo,1 Soghra Rabizadeh,1 Hamid Alemi,1 Salome Salehi,1 Reza Majdzadeh,2 Hossein Mirmiranpour,1 Assadollah Rajab, Alireza Esteghamati1 and Manouchehr Nakhjavani1

1Endocrinology and Metabolism Research Center, Vali-Asr Hospital, School of Medicine, Tehran University of Medical Sciences, Tehran, Islamic Re- public of Iran (Correspondence to: M. Nakhjavani: [email protected]). 2Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran.

Abstract Background: Proper glycaemic control can slow progression of diabetes complications. One of the main causes of poor glycaemic control is delayed initiation of insulin therapy. Aims: To explain the reasons for delayed insulin initiation based on a behavioural model using patients’ innate psychological needs. Methods: We enrolled 151 patients with type 2 diabetes who had indications for insulin therapy. Thirty general practitioners (GPs) were included as care providers. Patients were studied by questionnaires evaluating components of self determination theory, such as competency, relatedness and autonomy. We also evaluated patients’ attitudes towards insulin therapy using the Insulin Treatment Appraisal Scale questionnaire. GPs’ attitudes towards insulin therapy were assessed with a different questionnaire. Results: Competency of patients was scored as acceptable (14.44/20). Relatedness score was low at around 15.63/30. The findings suggested that the patients’ intrinsic motivation was less than their extrinsic motivation (8.41/15 vs 15.03/20). The main barrier to insulin therapy on the patients’ side was rejection of severity of illness (67.5%). According to GPs, low compliance (96.7%) was the main cause of delayed insulin prescription. Conclusions: We observed that patients do not have a proper understanding about their illness. Due to the low score of relatedness as a representative of patients and care providers’ relationship, we highlight the importance of educating both about insulin therapy and how they can have the most effective relationship in this process. Keywords: type 2 diabetes, insulin therapy, psychological aspects, self-determination theory, education Citation: Rajab A; Khaloo P; Rabizadeh S; Alemi H; Salehi S; Majdzadeh R; et al. Barriers to initiation of insulin therapy in poorly controlled type 2 diabetes based on self-determination theory. East Mediterr Health J. 2020;26(11):1331–1338. https://doi.org/10.26719/emhj.20.027 Received: 11/6/18; accepted: 25/03/19 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 Therefore, in the current study, we aimed to investigate Iranian patients’ and care providers’ attitudes that delay Diabetes has become one of the biggest global health initiation of insulin therapy. There are many behavioural issues, due to its rapidly growing prevalence, complica- models that can be used to analyse patients’ compliance tions and high burden of disease (1). Analyses from differ- and self-management ability. Self-determination theory ent countries including the Islamic Republic of Iran have (SDT) is one the most appropriate models that can be used demonstrated poor glycaemic control of diabetes in most in patients with diabetes. SDT is an approach to human patients (2). One of the main causes of poor glycaemic motivation and personality that uses innate psychological control is delayed initiation of insulin therapy (3–5). needs, including competence, relatedness and autonomy, The negative attitudes expressed by patients are fear which appear to be essential for optimal functioning of needles, self-blame for needing insulin, cost of insulin and social well-being (14,15). Previous research based on and doubts about efficacy (6,7). In addition, doctors SDT has revealed an association between medication prefer to postpone prescription of insulin, which is a adherence and autonomy and competence in chronic manifestation of clinical inertia (6,8,9). Clinical inertia disease. In the present study, we used SDT to explain why is defined as the failure of providers to alter therapy in patients refuse to initiate insulin therapy. the face of clear indications (6), and it is suggested causes include limited experience and knowledge along with Methods lack of standardized guidelines (10,11). Epidemiological shift from acute to chronic diseases Participants has required a new vision in treatment (12). In the This was a descriptive cross-sectional study in 5 general acute-care system, patients surrender a lot of control to medical clinics in Tehran, Islamic Republic of Iran in the healthcare providers. Diabetes care requires patients and summer of 2016. We randomly recruited 151 patients with healthcare providers to collaborate in development of poorly controlled type 2 diabetes who were candidates self-management plans (13). for insulin therapy according to the 2016 American Dia-

1331 Research article EMHJ – Vol. 26 No. 11 – 2020 betes Association/European Association for the Study of (19). Five experts including endocrinologists, diabetes Diabetes (ADA/EASD) guidelines. There were 89 women educators and an epidemiologist gave their opinion re- (58.9%) and 62 men (41.1%), aged 29–88 (mean 56.7) years. garding comprehensiveness, relevance and clarity of the Despite their need to start insulin therapy, none of the questionnaires. They were asked to evaluate the content patients had begun. Thirty general practitioners (GPs) validity ratio for the necessity of each item in the ques- (18 female, 12 male; mean age 37.6 years, age range 29–54 tionnaires, and to investigate the specificity and clarity of years) were selected randomly from general medical clin- each item using a 4-point Likert scale. After these steps, ics to estimate their attitude towards insulin therapy. We updated questionnaires were arranged in the presence of chose GPs rather than specialists because in the Islamic 5 patients attending the initial session and the question- Republic of Iran, most people go to general medical clin- naires were reviewed for revalidation. ics and are assessed by GPs. Also, national clinical guide- Changes in questionnaires and validation lines recommend that GPs are responsible for initiating insulin therapy or referring patients to specialists. There- The PCDS questionnaire was unchanged. It was decided fore, most patients with type 2 diabetes are under treat- to use the short form of the HCCQ questionnaire. The ment by GPs in the Islamic Republic of Iran. TSRQ questionnaire was revised to “Estimation of In- ternal Motives and Control Motives”, including 3 items Study design for determining internal motivations and 4 to estimate The study was divided into 2 parts: evaluation of patients’ external (control) motivations. In these 3 questionnaires compliance with insulin therapy, and evaluation of GPs it was intended to use the 5-point instead of 7-point Lik- attitudes to insulin therapy. All of the questionnaires ert scale. Thus, the total score of the questionnaires was were filled out by patients in the presence of a trained as follows: PCDS (4–20); short HCCQ (6–15); internal GP to help them better understand the questionnaires. motivation (3–15); and external motivation (4–20). For Data for demographic characteristics, pertinent clinical the ITAS questionnaire, positive attitudes (4 items) were information and exposure to insulin therapy were col- excluded, and instead, only 1 item was asked from the lected from the patients. GPs were also asked to fill in a patients to answer in the 3-point Likert scale. Two more questionnaire in the presence of another GP trained in negative attitudes were added to other items: (1) perhaps the procedure of filling in the form. This study received in the future insulin will become rare, for example, as a ethical approval from the Medical Research and Ethics consequence of economic sanctions, and (2) insulin ther- Committee, Tehran University of Medical Science. apy is more expensive than oral therapy), and patients were asked to agree or disagree. This questionnaire is Patients’ questionnaires also called R-ITAS (a modified version) and can illustrate the frequency of negative aspects of insulin therapy, To measure the components of SDT, some well-known which are the issues that patients feel or believe would questionnaires were used. (1) Perceived Competence in act as barriers to accepting insulin therapy. Diabetes Scale (PCDS), which measures by 4 items the competency of patients in controlling their diabetes Some additional questions were added based on the (16,17). (2) Health Care Climate Questionnaire (HCCQ), results of the above process and literature review (20), which measures by 15 items the support of the health including whether patients were recommended to accept system to improve patients’ autonomy. It also has a short insulin therapy by their healthcare provider, and whether form (containing 6 items) that is strongly correlated with any of their acquaintances were receiving insulin the full version and highly reliable (16,17). (3) The Treat- therapy. The other question was based on the number of ment Self-Regulation Questionnaire (TSRQ) contains 2 visits of patients to physicians in a year. Their attitude sections (19 items) to estimate the intrinsic and extrinsic towards seriousness of diabetes and risk of developing motivators of controlling diabetes, displaying autono- its complications was measured on a 5-point Likert scale mous versus controlled regulation of behaviour (17). (5) (1, very low and 5, very high). Insulin Treatment Appraisal Scale (ITAS) contains 20 GPs’ questionnaire items measuring the positive and negative attitude of patients to insulin therapy (18). The same procedure was used for GPs to prepare a questionnaire containing questions including: (1) trying to Revising the questionnaires understand the reasons for not accepting insulin therapy All of the above questionnaires were in English and had from the patients’ perspective when GPs put themselves not been translated into Persian before this study; therein the patients’ place; (2) reasons for delaying or not ad- fore, after translation, a qualitative study was done to ministering insulin therapy by physicians; and (3) GPs consider the effects of social and cultural differences. familiarizing themselves with clinical guidelines in this Then, a group session with 15 type 2 diabetes patients area and determining the therapeutic goals based on the was held to decide about the appropriate questions and guidelines. The validity and reliability of the GPs’ ques- items. After summarizing the discussions by the trained tionnaire was assessed by the above-mentioned proce- GP, participants were asked to confirm the items in or- dure. The internal consistency of the questionnaire for 10 der to increase the credibility and conformability of the GPs was measured α = 0.78 (P < 0.001). The trained GP items. To perform content validation for development who was involved in the patients’ questionnaires study of new questionnaires, we followed Abdollahpour et al. was not included in the GPs’ questionnaire study.

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Data analysis Table 1 Demographic findings Data were collected and analysed by SPSS version 21 sta- Characteristics No. % tistical software. The relationships between psychomet- Sex ric factors and demographic findings were evaluated by Male 62 41.1 appropriate statistical tests, such as t test, Mann–Whit- Female 89 58.9 ney test and Spearman correlation analysis for nonpara- Education metric variables, and Pearson correlation analysis. Tests Illiterate 10 6.6 of normality were performed by Kolmogorov–Smirnov test. Many of the distributions were not normal, includ- Below diploma 85 56.3 ing PCDS, HCCQ, and intrinsic motivation and extrinsic Diploma 34 22.5 motivation (obtained from modified TSRQ), (all P < 0.001), Higher education 22 14.6 so nonparametric signed rank tests were run. P < 0.05 Mean annual income (US$) was considered statistically significant. < 2400 14 9.3 2400–4200 82 54.3 Results > 4200 55 36.4 Physician level of practice Baseline characteristics General practitioner 83 55 The average number of checkups per year for the 151 Internist (Endocrinologist) 68 45 patients was 3.14, with significantly more in women Long-term complications (P = 0.002). The mean time that doctors spent on a patient Yes 40 26.5 in a usual visit was < 5 minutes. Only 73 patients (48.3%) were recommended to initiate insulin therapy. This No 111 73.5 number was significantly lower in patients who were un- Family history of type 2 diabetes der supervision of a GP [odds ratio (OR) = 5.56, P < 0.001, Yes 99 65.5 χ2 = 25.4]. Forty (26.5%) patients developed diabetes com- No 52 34.4 plications (Table 1). Family history of insulin treatment Baseline fasting blood sugar, haemoglobin A1c Yes 59 39.1 concentration, body mass index (BMI), systolic and No 92 60.9 diastolic blood pressure, and duration of diabetes are shown in Table 2. Mean BMI was significantly higher in female patients (P < 0.001, t = 10.99). Patient attitudes toward insulin therapy We asked patients to score the seriousness of diabetes out of 5 (1, very low and 5, very high). The mean score was Based on the findings of the R-ITAS questionnaire de- 3.44. Only 17 (11.3%) patients described diabetes as having veloped from modification of ITAS, the following results were obtained. Only 39 (25.8%) patients believed in insu- low seriousness. We also asked patients to evaluate their lin efficacy; 82 (54.3%) did not have enough knowledge; risk of developing diabetes complications by giving a and 30 (19.9%) thought that insulin was ineffective for risk score of 1 (very low), 2 (low), 3 (moderate), 4 (high) treatment of diabetes. The most common reasons for or 5 (very high). The number of patients in each category patients refusing insulin therapy are shown in Figure 1. was 73 (48.3%), 52 (34.4%), 12 (7.9%), 13 (8.6%) and 1 (0.7%), The main reason was that they did not believe in the se- respectively. Mean score was 1.79. verity of their disease. Only 26 (17.2%) patients were wor- Psychometric findings ried about hypoglycaemia after initiating insulin therapy and it was not one of the common reasons of avoiding The results for PCDS, HCCQ and modified TSRQ (intrin- insulin therapy. Fear of needles (P = 0.02, t = 3.25) and sic and extrinsic motivation) are shown in Table 3. There difficulty with injecting the right amount of insulin was no significant difference in controlled motivation, (P = 0.035, t = 3.16) were more prevalent in older patients. self-motivation and perceived competence between pa- The number of patients who agreed with insulin efficacy tients who were under supervision of a GP compared (n = 16; 27.1%) was significantly lower among those who with an internist. HCCQ scores were significantly higher knew another patient using insulin (P < 0.001). Patients in patients working with an internist (P = 0.003, z = 2.94) with lower level of education, including illiteracy and be- and had a positive correlation with the time doctors spent low diploma level (n = 53; 55.8%), believed that they did in a usual visit (P < 0.001, z = 5.78). Self-motivation scores not have enough knowledge about whether insulin was were also higher in this group. Age had an inverse cor- effective, compared with patients with higher level of relation with PCDS (P < 0.001) and a positive correlation education (n = 23; 41.0%) (P = 0.049, χ2 = 9.57). Patients with controlled motivation (P < 0.001; r = 0.31). HCCQ, with lower level of education agreed more than others self-motivation and PCDS scores were lower in patients that managing insulin injections takes a lot of time and with diabetes complications (P < 0.001, z = 2.4; P < 0.001, energy (OR = 2.44, 95% confidence interval = 1.14–5.2, P = z = 2.55; P = 0.011, z = 4.47, respectively). 0.012, χ2 = 6.30).

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Table 2 Baseline characteristics Characteristics Minimum Maximum Mean SD FBS (mg/dl) 54 597 183.73 74.96 HbA1c (%) 7.50 14.60 9.42 1.11 BMI (kg/m2) Male 13.29 54.09 27.08 4.39 Female 15.06 54.09 29.38 5.17 SBP (mmHg) 91 207 132.99 20.64 DBP (mmHg) 51 130 79.53 11.76 Duration of diabetes (yr) 1 30 8.46 5.61 BMI = body mass index; DBP = diastolic blood pressure; FBS = fasting blood sugar; HbA1c = haemoglobin A1c; SBP = systolic blood pressure; SD = standard deviation.

GP attitudes insulin therapy. This highlights the importance of injection stigma and how it affects the proper treatment of di- From the GPs’ perspective, the most common reasons for patient refusal of insulin are shown in Figure 2. The abetes. Other reasons expressed by participants included most common reasons for GPs delaying insulin prescrip- difficulties in fulfilling daily responsibilities and difficul- tion were: expectation of low patient compliance (n = 29; ties with injecting the right amount of insulin. 96.7%); fear of hypoglycaemia (n = 25; 83.3%); insulin is Doctors assumed that fear of needles and the pain the last choice of therapy (n = 20; 66.7%); and lack of suit- caused by injection were the main reasons for rejecting able guidelines and training (n = 16; 53.3%). Twenty-four insulin therapy among patients; however, as mentioned GPs believed they needed to refer patients to an internist before, patients feel embarrassed about insulin injection or endocrinologist for insulin initiation, while the other and are not necessarily frightened of it. In our study, 6 believed that they were able to initiate insulin therapy 51.7% of patients were not recommended to take insulin by themselves. Only 11 GPs managed diabetes based on at all despite the medical indicators showing a significant standardized guidelines (ADA/EASD), and only 5 had read need for it. Care providers should endeavour to explain up-to-date guidelines. more thoroughly the benefits of taking insulin and try to make patients comfortable with starting treatment early. Discussion This would break the cycle of clinical inertia. This is more common among patients who are under supervision We aimed to determine the barriers to initiation of in- of a GP (22). Our study showed similar results. Low sulin therapy in patients with type 2 diabetes, who had compliance and high possibility of hypoglycaemia were clear indications for starting insulin therapy but were the main reasons GPs expressed for avoiding insulin not using insulin. Our results showed that more than half of our patients did not have enough knowledge about in- prescription. We observed that just 17.2% of patients sulin efficacy. This is one manifestation of inadequate were worried about hypoglycaemia as a result of insulin knowledge of patients about diabetes (21). Only 17.2% of therapy compared to 83.3% of GPs. The reason could be patients found themselves at risk of diabetes compli- lack of knowledge of people about insulin therapy and the cations. Denial of the severity of the disease and denial risk of hypoglycaemia. It requires more complete future of the failure of oral agents were the main reasons for investigation in the future. Since most patients with refusing insulin therapy among patients. It means that diabetes attend GPs for treatment (23) we need to educate they cannot accept that their disease has progressed. This GPs and establish standardized guidelines. A significant can be explained by the chronic nature of diabetes and majority (63.3%) of our participants complained about a the delayed appearance of complications. In other words lack of national guidelines for diabetes treatment. There patients do not worry about the future consequences of are clinical guidelines discussing the principles needed the disease because they feel healthy at the present time. to be considered by doctors in every visit, although many Patients’ belief that injecting insulin is embarrassing was doctors do not have access to these guidelines; therefore, another noticeable reason for their delaying initiation of they may be neglected in usual visits (10,24).

Table 3 Psychometric findings Minimum Maximum Mean SD PCDS 4 19 14.44 3.15 HCCQ 6 28 15.63 4.67 Intrinsic motivation 4 14 8.41 2.51 Extrinsic motivation 5 19 15.03 2.7 HCCQ = Health Care Climate Questionnaire; PCDS = Perceived Competence in Diabetes Scale; SD = standard deviation.

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Figure 1 Common reasons for patients refusing insulin

Ongoing loss of personal health

Difﬁculty of timely and correctly use of insulin

Interference with activities of daily living

Embarrassment about injection

Denial of failure of treatment with oral agents

Denial of disease severity

0 10 20 30 40 50 60 70 80 % Data presented in bars as percentage (number of cases)

Psychometric findings showed a reasonable score patients improves the latter’s attitude (27). A low HCCQ (14.4/20) for PCDS. This index indicates the competency score indicates poor insight of doctors about diabetes of diabetic patients to control their disease (25). Our treatment and the fact that they should play the role results demonstrated an inverse association between age of counsellor for patients (13). We found similar results and PCDS score. This indicates that ageing has a negative in our study since the reasons patients expressed for impact on how patients feel about their competence in refusing insulin therapy varied from those doctors self-management. These results confirm previous studies assumed. Grant et al. described the negative impacts of (26). Older patients need more help in order to enhance these prejudgments on initiation of insulin therapy (29). this index, especially for complicated procedures such as We studied the components of TSRQ index including insulin therapy. intrinsic motivation and extrinsic motivation separately. Contrary to PCDS index, the mean HCCQ score was Extrinsic motivations were significantly higher compared not positive enough. It was almost half of the maximum to intrinsic motivations; however, it is reported that score. This index reflects the relationship between care intrinsic motivation is more important for initiation of providers and patients and how healthcare systems and adherence to insulin therapy (17). Extrinsic motivation support patients for self-management (27). Numerous on its own can be counterproductive. It is necessary for studies have suggested that low HCCQ score and poor the internalization of the requested behaviour but if the communication with care providers could be one of internalization does not occur properly it can make the the reasons for patients refusing insulin therapy (27). patients disappointed rather than motivated (14,15). In Moreover, low HCCQ score aggravates the negative our study intrinsic motivations had the lowest scores attitudes toward insulin therapy among patients (28). among SDT parameters. That is because patients do A well-established relationship between doctors and not find themselves at risk of diabetes complications.

Figure 2 Common reasons for patients refusing insulin from general practitioners’ point of view

Denial of disease severity

Pain of injection

Interference with responsibilities

Difﬁculty of adjusting insulin dose

Fear of injection

0 20 40 60 80 100 % Data presented in bars as percentage (number of cases)

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It is reported that this issue can minimize patients’ energy. These results may explain the self-confidence of motivation to initiate more-intensive therapies such as patients with higher level of education. insulin therapy (30). There were some limitations to our study. First, One particularly interesting finding of our study was benchmark scores for the questionnaires have not that patients who knew a person using insulin did not yet been determined in the Islamic Republic of Iran. believe in insulin efficacy. It can be explained by the poor Therefore, we tried just to show the components of SDT glycaemic control of patients when initiating insulin among Iranian patients themselves. Second, we were not therapy (3,31). In other words, patients who accept insulin able to evaluate the general knowledge of our participants therapy are those who are at later stages of the disease but about diabetes because of low cooperation and large people suppose that insulin has caused complications. number of questionnaires. Third, we only included GPs We showed that participants with lower compared as care providers. with higher educational level had uncertainty about the In conclusion, initiation of insulin therapy is efficacy of insulin therapy. However, agreement about efficacy of insulin therapy among participants with dependent on multiple factors. We observed that patients higher education level was not as high as we expected. do not have a proper understanding of their illness and Perhaps these findings are based on the fact that patients require improved intrinsic motivation. Care providers do with low and high education level had little knowledge not have an accurate understanding of what the patients’ about diabetes and its treatment, although the latter psychological barriers to treatment are. Our study group had more definite opinions. In addition, highly highlights the importance of educating both patients and educated patients disagreed more with the idea that care providers about insulin therapy and how they can managing insulin injections takes a lot of time and have effective communication in this relationship.

Acknowledgement The authors wish to thank all patients for their participation and kind cooperation. Funding: None. Competing interests: None declared.

Obstacles face à la mise en place de l’insulinothérapie dans le diabète de type 2 mal contrôlé selon la théorie de l’autodétermination Résumé Contexte : Un contrôle adéquat de la glycémie permet de ralentir la progression des complications du diabète. Le retard dans la mise en place de l’insulinothérapie constitue l’une des principales causes d’un mauvais contrôle de la glycémie. Objectifs : Expliquer les raisons du retard de la mise en place du traitement par insuline sur la base d’un modèle comportemental fondé sur les besoins psychologiques innés des patients. Méthodes : Nous avons recruté 151 patients atteints de diabète de type 2 pour lesquels l’insulinothérapie était indiquée. Une trentaine de médecins généralistes ont été inclus en qualité de prestataires de soins. L ’ étude a été menée au moyen de questionnaires évaluant des composantes de la théorie de l’autodétermination, telles que la compétence, l’affiliation et l’autonomie. Nous avons également évalué les attitudes des patients vis-à-vis de l’insulinothérapie à l’aide du questionnaire de l’échelle d’évaluation de l’insulinothérapie (Insulin Treatment Appraisal Scale). Les attitudes des médecins généralistes vis- à-vis de l’insulinothérapie ont été évaluées au moyen d’un questionnaire différent. Résultats : La compétence des patients a été jugée acceptable (14,44/20). Le score se rapportant à l’affiliation était faible, à environ 15,63/30. Les résultats suggèrent que la motivation intrinsèque des patients était inférieure à leur motivation extrinsèque (8,41/15 contre 15,03/20). Du côté des patients, le rejet de la gravité de la maladie (67,5 %) constituait le principal obstacle à la mise en place de l’insulinothérapie. Selon les médecins généralistes, une faible observance (96,7 %) était la principale cause de retard dans la prescription d’insuline. Conclusions : Nous avons observé que les patients ont une mauvaise compréhension de leur maladie. En raison de la faiblesse du score concernant l’affiliation, en tant qu’élément représentant la relation entre les patients et les prestataires de soins, nous soulignons l’importance d’une meilleure sensibilisation des malades et soignants à l’insulinothérapie et de la manière de mettre en place une relation efficace.

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العوائق التي َ ُتول دون بدء العالج باألنسولني لداء ُّالس َّ ريك من النمط الثاين الذي ال يمكن ضبطه ًجيدا ًاستنادا إىل نظرية تقرير املصري أرمنيرجب، بيجا خالو، صغرى رايب زاده، محيد العليمي، سالومي صاحلي، رضا جمدزاده، حسني مريمريانبور، أسد اهلل رجب، عيل رضا إستغامايت، منوچهر نخجواين اخلالصة اخللفية: يمكن أن يؤدي ضبط سكر الدم عىل ٍ نحوصحيح إىل إبطاء تفاقم مضاعفات ُّالس َّكري. ُعد ويتأخر بدء العالج باألنسولني أحد األسباب الرئيسية التي حتول دون الضبط اجليد لسكر الدم. األهداف: هدفت هذه الدراسة إىل رشح أسباب ُّتأخر بدء العالج باألنسولني بِ ً عىلناء نموذج سلوكي يستند إىل احتياجات املرىض النفسية الفطرية. طرق البحث: شملت هذه الدراسة 151 ًمريضا ُّبالس َّ ريمن كالنمط الثاين تستدعي حاالهتم العالج باألنسولني. وشملت ثالثني ًممارسا ًعاما يضطلعون بدور ُم ِّقدمي خدمات الرعاية. وخضع املرىض للدراسة عن طريق استبيانات لتقييم ِّناتمكو نظرية تقرير املصري، مثل الكفاءة واالرتباط واالستقاللية. كام أجرينا ًتقييامملواقف املرىض جتاه العالج باألنسولني باستخدام استبيان مقياس تقييم العالج باألنسولني. ُوق ّي َمت مواقف املامرسني ِّني العامجتاه العالج باألنسولني باستخدام استبيان خمتلف. النتائج: حصلت كفاءة املرىض عىل درجة مقبولة )14.44/ (، 20فيام حصل االرتباط عىل درجة منخفضة ُت َّقدر بنحو 15.63/30. وأشارت النتائج إىل أن الدافع الذايت للمرىض كان َّ أقلمن دوافعهم اخلارجية )8.41/15 مقابل 15.03/20(. َوت َّثل العائق الرئييس الذي ُحيول دون إقدام املرىض عىل العالج باألنسولني يف عدم االعرتاف بشدة املرض )67.5٪(. َوو ْف ًقا للمامرسني ِّالعامني، كان انخفاض االمتثال )96.7%( السبب الرئييس ُّلتأخر وصف األنسولني. االستنتاجات: الحظنا أن املرىض ال يتمتعون ٍبفهم ٍصحيح ملرضهم. ً ونظراالنخفاض درجة االرتباط كممثل للعالقة بني املرىض ُوم ِّقدمي خدمات الرعاية، فإننا ُن ّسلط َالضوء عىل أمهية تثقيف ٍكل منهام بشأن العالج باألنسولني، وكيف يمكن الوصول إىل أفضل عالقة ّالةفع بني الطرفني يف إطار هذه العملية.

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Prevalence of non-reporting of hospital medical errors in the Islamic Republic of Iran

Mehrdad Askarian,1 Seyyed M. Sherafat,2 Maryam Ghodsi,3 Zahra Shayan,4 Charles Palenik,5 Nahid Hatam6 and Yavor Enchev7

1Department of Community Medicine, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran; Health Behavior Science Research Center, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 4Trauma Research Center, Department of Community Medicine; 2Student Research Committee; 6Department of Health Service Administration, School of Management and Information Sciences, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran (Correspondence to: Mehrdad Askarian: [email protected]). 3Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 5School of Dentistry, Indiana University, Indianapolis, United States of America. Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 7Department of Neurosurgery, University Hospital St. Marina, Medical University of Varna, Varna, Bulgaria..

Abstract Background: Medical errors frequently occur in health care facilities, jeopardizing patient safety and increasing associated costs. Aims: This cross-sectional investigation examined the rates of and reasons for non-reporting of medical errors at Nema- zee Hospital, Shiraz, Islamic Republic of Iran. Methods: Self-administered questionnaires were completed by 283 staff members, including physicians, nurses and medical students. One-way analysis of variance, Fisher’s least significant difference post hoc, Spearman correlation coefficient and intraclass correlation tests were used for statistical analyses. Results: Almost all (95.8%) participants had observed at least 1 medical error during the previous year, with over half (50.5%) observing 3–10 errors. The preferred method for reporting medical errors among physicians and medical students was verbal and informal (40.3% and 41.8% respectively), while nurses preferred written forms (45.7%). The results indicated significant differences between groups concerning individual and organizational barriers in general, and among all sub-categories (P < 0.001). Conclusion: Concerns of legal entanglements and confidentiality issues were recognized as the main barriers to reporting medical errors. Keywords: medical errors, non-reporting, patient safety, hospitals, health care workers Citation: Askarian M; Sherafat SM; Ghodsi M; Shayan Z; Palenik C; Hatam N; et al. Prevalence of non-reporting of hospital medical errors in the Islam- ic Republic of Iran. East Mediterr Health J. 2020;26(11):1339–1346. https://doi.org/10.26719/emhj.19.050 Received: 20/06/17; accepted: 30/07/18 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 A survey in 6 South Australian hospitals reported that even though 98.3% of respondents were aware of their More than 16 years after the landmark report by the Insti- facility’s incident reporting systems, more than 40% had tute of Medicine, serious concerns about patient safety never filed a report (11). Another study reported 84.3% of continue to exist (1–3). Medical errors are estimated to be 338 internal medicine physicians and residents believed the third leading cause of death in the United States of that reporting medical errors improved quality. However, America (4). There have been 4 major studies conducted their rate for reporting minor errors was only 16.9% and since the Institute of Medicine study concerning deaths for major errors 3.8% (12). Understanding the multiple associated with medical errors. Together they cover over factors that influence reporting errors among health 37 million patient admissions with a 3.1% rate of adverse care workers is crucial to supplying missing elements of events and a 0.7% mortality rate (5–7). an effective communication programme. Such barriers Efficiency, security of care, care giver reactivity and can damage the transparency of a safety climate and a patient contentment are safety parameters that are culture of learning from errors (8,13,14). at the core of health care quality (3). The most crucial A perfectionist belief is that only poor physicians factor, however, is a comprehensive understanding of make mistakes (2,13). Several studies indicate that there medical errors (8). Gathering meticulous evidence via is a lack of knowledge concerning reportable incidences. transparent incident reporting, free sharing of data and Many physicians and nurses often do not consider near the creation of a culture of learning from our mistakes misses and medication omissions as being reportable (2). are indispensable in the development of medical error In one study, 25% of participants did not know how to reduction plans and improving patient safety (2,5,9). The retrieve their facility’s incident reporting form (11). backbone of the movement towards an enhanced culture At the institutional level, the safety climate often of safety is a well-organized error reporting system (10). determines front-line provider attitudes (13). Loss of

1339 Research article EMHJ – Vol. 26 No. 11 – 2020 malpractice insurance coverage, fear of punitive actions, a pilot study), precision of 0.25, population of 2000 and time constraints, poorly designed reporting systems, considering withdrawal proportion of 25%. negative feedback, lack of confidentiality and a power The study population was selected randomly from hierarchy within professional groups are factors that available personnel in all 32 wards in the hospital and negatively affect error reporting (2,8,13,14). Other factors during all shifts. Questionnaires were presented in can be even more specific, such as fear of disciplinary written form and completed immediately during a action and threats to positive evaluations and promotion, break in the shift and took 10 minutes on average. The especially among nurses (2,13,15). questionnaire used in this study was developed by a In a study of 20 hospitals in the north of the Islamic hospital study group. A group of topical experts then Republic of Iran, 182 (0.06% of 317 966 admissions) medical assessed the questionnaire for content validity. The errors were reported. The lack of a reliable reporting questionnaire was piloted on 19 medical students and 17 system, negative attitudes toward reporting among staff nurses in the study group. Cronbach’s alpha calculation and managers and a punitive culture were mentioned as was used to assess reliability. The resulting value was the potential causes (16). The rate of non-reporting was 0.819. estimated at 78.9% within the nursing staff of a teaching The first section of the questionnaire covered hospital in Kermanshah (17). There were comparable demographic characteristics, including sex, work results in 2 other independent surveys among nurses at experience and department. The second section Imam Khomeini Hospital in Tehran (18,19). contained questions about participant knowledge Barriers to medical error reporting were investigated concerning medical errors, past in-service training, among health care providers in the Islamic Republic number of witnessed errors during the previous year, of Iran in 2012. The study reported a high incidence preferred method for reporting errors and response to of mishaps with lower rates of reporting (< 50%). The medical errors committed, either by themselves or their absence of an effective medical error reporting system, peers. an insufficient supporting atmosphere among peers, Barriers to medical error reporting were assessed lack of sufficient knowledge regarding the importance through 13 statements involving personal and of error reporting and fear of malpractice litigation were organizational opinions and behaviours. Participants listed as the most common impediments (20). reported their level of agreement using a scale of 1–10. In the summer of 2014, a web-based error reporting Unfamiliarity with medical errors or the reporting system was launched at Nemazee Hospital in Shiraz. process, fear of punishment, cultural issues within Reporting forms were revised and multiple training a group, lack of confidentiality, a time-consuming courses presented. Following these efforts, error reports reporting system, lack of proper feedback and fear of increased by approximately 2000 cases per month. malpractice lawsuits were considered as organizational However, topical specialists felt that there was still factors. There were 4 additional questions that addressed room for improvement. Also, there was a strong need respondent knowledge about medical errors. to compare the effectiveness of the Nemazee Hospital Statistical analyses programme with others currently operating in the Islamic Republic of Iran. Therefore, the aims of this study were to Analysis included descriptive analysis, 1-way analysis of determine the reasons behind non-reporting by hospital variance, Fisher’s least significant difference post hoc, in- staff physicians, nurses and medical students and how traclass correlation (ICC) test. SPSS, version 23, was used. well the facility error reporting is actually operating. P-value < 0.05 was considered significant. Ethical considerations Methods The protocol of this study was approved by the Shiraz Study setting University of Medical Sciences research ethics committee (IR.SUMS.MED.REC.1394.S01). Participation was vol- We conducted a cross-sectional descriptive study from untary. September–December 2015 in Nemazee Hospital, Shiraz, Islamic Republic of Iran. The facility is a general, specialty and subspecialty teaching hospital with 750 beds and Results is considered as the main referral centre in the south of Participants included 151 nurses (53.3%), 77 physicians the country. (27.2%) and 55 medical students (19.4%). The largest group of participants [53 nurses (35.1%), 41 physicians (53.2%) Questionnaires and 23 medical students (41.8%)] worked in internal med- Data were collected from 283 participants (82% response icine units; 62 nurses (41.1%) and 31 physicians (40.2%) rate), including physicians, nurses and medical students had less than 5 years of work experience. Witnessing at using a self-administered questionnaire. Samples were least 1 error during the previous year was reported by 271 selected with a confidence level of 95%, standard devia- (95.5%) respondents. More than half (143, 50.5%) had ob- tion 2 (score of barriers against error reporting based on served 3–10 medical errors in the previous year (Table 1).

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Table 1 Distribution of observed medical errors among physicians, nurses and medical students (n = 283) during 2015 in Nemazee Hospital, Shiraz , Islamic Republic of Iran Occupation No. of times seen Not seen (%) 1–2 (%) 3–10 (%) > 10 (%) Physician 1.3 23.4 54.5 20.8 Nurse 7.3 31.1 45.0 16.6 Medical student 0.0 20.0 60.0 20.0 Total 4.2 26.9 50.5 18.4

Physicians (n = 31, 40.3%) and medical students (n = 23, study participants; 55 physicians (71.4%) and 24 medical 41.8%) preferred to report errors via a telephone call or in students (43.6%) reported having no or inadequate person to a supervisor. However, nurses favoured using training on errors(n = 59, 76.6%) and error reporting written forms to report an error (n = 69, 45.7%). (n = 39, 70.9%). Conversely, most nurses reported that they Among physicians, 32 (41.6%) stated that “they would had received adequate training on error identification report only themselves, believing reporting superiors (n = 89, 58.9%) and error reporting (n = 98, 64.9%). would be considered offensive.” Among nurses, 54 (35.8%) The second part of the questionnaire contained believed that “It is mandatory to report all witnessed 13 statements regarding possible obstacles to error errors to a supervisor”. The largest group of medical reporting. The analysis of variance test indicated students (n = 21, 38.2%) indicated that “It is mandatory to significant differences between groups concerning disclose if the committed error is significant (e.g. vitally individual barriers in general and among all sub- important)”. categories, with nurses having the highest mean score Knowing the person making an error would not for all categories (Table 2). The least significant difference influence the decision to report for 38 physicians (49.4%), post-hoc analysis showed statistically significant 120 nurses (79.5%) and 31 medical students (56.4%). To differences between nurses and physicians (P < 0.001) measure agreement of actual information level and the and nurses and medical students (P < 0.001). Similarly, self-perception of participants, we calculated group ICC significant differences existed among the 3 study groups indices: most correlations were weak. The degree of concerning organizational barriers in general and among consistency among physicians (ICC = 0.06) was less than all sub-categories (again, nurses had the highest mean for nurses (ICC = 0.39) and medical students (ICC = 0.38). score in each category) (Table 3). The questionnaire also assessed the impact that Barriers most often mentioned by physicians were hospital-provided medical error training courses had on “Worrying about the revelation of a colleague’s identity”,

Table 2 Score distribution for individual barriers to error reporting among physicians, nurses and medical students (n = 283) in Nemazee Hospital, Shiraz, Islamic Republic of Iran, 2015 Barrier Mean (range 0–5) SD P-value Individual (overall) Physicians 1.8 0.4 < 0.001 Nurses 3.6 1.7 Medical students 1.9 0.3 Unfamiliarity with medical error/reporting process Physicians 1.7 0.5 < 0.001 Nurses 3.1 1.9 Medical students 1.8 0.5 Fear of punishment Physicians 2.1 0.7 < 0.001 Nurses 4.6 3.0 Medical students 2.3 0.6 Cultural issues Physicians 1.6 0.5 < 0.001 Nurses 3.2 1.9 Medical students 1.5 0.4 P-value is estimated based on 1-way analysis of variance test. SD = standard deviation.

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Table 3 Score distribution of organizational barriers against error reporting among physicians, nurses and medical students (n = 283) in Nemazee Hospital, Shiraz, Islamic Republic of Iran, 2015 Barrier Mean SD P- value Organizational (overall) Physicians 2.1 0.5 < 0.001 Nurses 4.4 2.2 Medical students 2.1 0.4 No confidentiality Physicians 2.0 0.7 < 0.001 Nurses 4.1 3.1 Medical students 2.0 0.7 Time consuming reporting system Physicians 2.0 0.8 < 0.001 Nurses 4.3 3.1 Medical students 1.9 0.8 Lack of proper feedback Physicians 2.2 0.8 < 0.001 Nurses 4.5 2.2 Medical students 2.2 0.7 Fear of malpractice lawsuit Physicians 2.2 0.8 < 0.001 Nurses 4.7 3.4 Medical students 2.2 0.7 P-value is estimated based on 1-way analysis of variance test. SD = standard deviation.

“Fear of a malpractice lawsuit” and “An inefficient error suggested physicians were more likely to report major reporting system”. The top issue for nurses and medical medical errors than other health care workers (9). Our students was “Worry about being criticized by peers or findings are comparable to surveys in that demographic supervisors” (Table 4). characteristics, especially work experience and assigned wards among nurses, did not influence medical error Discussion reporting (13). The informal reporting style of physicians has been Medical errors remain a serious health concern world- noted in other studies (9,14). Nurses favoured more wide and require special attention by health care admin- formal reporting schemes for all types of errors. All 3 of istrators and policy-makers (5,10). Health care providers our groups indicated their rate of reporting was the same are often reluctant to report patient safety problems, if the error was theirs or that of a colleague. However, which could jeopardize proper medical error reporting Alsafi et al. indicated that almost one-third of physicians (13). This study was designed to assess the main impedi- would not report a peer to preserve their relationship (9). ments against error reporting among physicians, nurses In our study, the ranking of barriers was different and medical students in Nemazee Hospital. between the groups. Fear of legal complaints, reproach, We found that almost 96% of respondents had punishment, lack of positive feedback, concern for observed an error at least once during the previous endangering a colleague’s occupational status or year. This agrees with an American study in which 94% revelation of his/her identity were often reported. of physicians and 88.7% of other health care workers In contrast, items such as “Errors are unavoidable in witnessed one or more medical errors in their department medical practice” and “There was nothing serious to (12). The majority (98%) of anaesthetists who participated report” received the lowest scores. However, a study from in a similar study conducted in Switzerland disclosed Australia reported conflicting results (24). being involved with a medical error (7). Fear of legal consequences was among the top reasons As in other studies, we found that nurses were more for non-reporting by physicians, nurses and medical inclined to report medical errors than were physicians students. Legal repercussions have been recognized as one and students. Physicians perceived more barriers against of the most pervasive obstacles to open communication proper reporting (21,22). One study indicated that only (25,26). A study of 733 nurses in Urmia, Islamic Republic of 42% of physicians routinely reported medical errors Iran, indicated that reproach and penalties were the most (23). Conversely, the findings of a Saudi Arabian study cited obstacles to proper reporting (26). A survey among

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Table 4 Barriers against error reporting among physicians, nurses and medical students (n = 283) in Nemazee Hospital, Shiraz, Islamic Republic of Iran, 2015 Items Physicians Nurses Medical students P-value Mean (SD) Mean (SD) Mean (SD) Not familiar with reportable issues 1.77 (0.74) 2.99 (2.67) 1.85 (0.7) < 0.001 Not familiar with error reporting ways 1.96 (0.79) 2.69 (2.64) 2.15 (0.8) 0.023 Worry about my identity revelation 1.95 (0.84) 3.70 (3.15) 1.82 (0.7) < 0.001 Worry about revelation of colleague’s identity 2.50 (0.81) 4.47 (3.42) 2.18 (0.61) < 0.001 It is a time-consuming process 2.00 (0.78) 4.34 (3.14) 1.93 (0.77) < 0.001 Fear of malpractice lawsuit 2.18 (0.84) 4.69 (3.36) 2.16 (0.69) < 0.001 Fear of penalty or job loss 2.13 (0.80) 4.43 (3.16) 2.27 (0.71) < 0.001 Worry about being criticized by peers or supervisor 2.03 (0.78) 4.73 (3.32) 2.33 (0.67) < 0.001 There was nothing serious to report 1.42 (0.59) 3.58 (3.06) 1.44 (0.57) < 0.001 Error reporting is not efficient 2.16 (0.80) 4.52 (3.25) 2.22 (0.74) < 0.001 Come on! Who wants to do such things? 1.70 (0.73) 3.08 (2.74) 1.64 (0.7) < 0.001 Error reporting is not a usual concern 1.81 (0.74) 3.62 (2.77) 1.62 (0.68) < 0.001 Error is unavoidable in medical practice 1.40 (0.61) 2.86 (2.61) 1.22 (0.50) < 0.001 SD = standard deviation. nurses from hospitals affiliated with Tehran and Shiraz and nurses do not receive adequate information (8). universities of medical sciences listed fear of legal action, Throckmorton et al. showed nurses could not identify job threats and a negative culture of blame as major errors in 40% of cases (29), although no practical scenario impediments (27). However, some studies, including was provided for the accurate assessment of medical one from the Netherlands, indicated that fear of legal error recognition and understanding in this study, and complaints was not a significant concern for internists there was evidence that 73.5% of nurses and almost half and residents reporting medical errors (8,28). of physicians and medical students had an inadequate Research carried out in the United States of America background on the topic. revealed that when anonymous reporting was established, Significant limitations of this study included nurses reported both minor and major medical errors voluntary participation, self-reporting of information at higher rates (29). In a Saudi Arabian study, 60% of and possible recall bias. Some participants might not physicians noted that reporting would be easier when have recalled their errors very well. This could result in there was a heightened level of confidentiality (9). Fear underestimation of the actual rate of reported medical of being identified was not a major concern in our study, errors. Also, correlation measurements between causes however, it was listed as one of the most discouraging of non-reporting and job titles of nurses, including factors concerning medical error reporting. supervisory, was not possible due to the limited number Time consumption was not a top-ranked factor against of supervisors and head nurses among our participants. proper medical error in our study nor in another from the Possible future studies could involve greater numbers Islamic Republic of Iran (26). More than 50% of Australian of participants and other types of health care workers. physicians and 40% of nurses felt their cumbersome Applying our questionnaire in other hospitals could also reporting system was an important barrier (30). A Swiss be worthwhile. It would be valuable if hospitals of various cross-sectional survey involving anaesthetists reported sizes were involved. not only sluggish reporting systems, but also inadequate feedback and lack of information negatively affected error reporting (8). Polisena et al. determined that more Conclusions than half of the physicians and nurses surveyed believed Concerns about legal entanglements, reporting method- their reporting system was incompetent and that they ology and confidentiality issues were recognized as the failed to receive plausible and timely feedback (30). Our main barriers to reporting medical errors in Nemazee study showed comparable results, which indicated that Hospital. Nurses did report errors at higher rates and ineffectiveness of the error reporting system was among they were found to prefer more formal, extensive, written the top 3 causes of non-reporting by physicians, nurses reporting forms and the inclusion of all types of errors. and medical students. Physicians and medical students preferred the opposite. The World Health Organization published a guideline Furthermore, the lack of knowledge on identifying and for medical students in 2009 which included 11 topics on reporting medical errors among physicians and medi- patient safety (31). A number of studies indicate that most cal students requires attention by hospital administers. medical students receive little information about medical It appears that a formal reintroduction of the reporting errors or reporting techniques (32,33), and staff physicians system with accompanying in-service training is needed.

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Acknowledgment This article is the result of a research project that was funded by the Vice-Chancellor for Research, Shiraz University of Medical Sciences, and carried out by Seyyed Mohammad Mahdi Sherafat in partial fulfilment of the requirements for certification as a general practitioner at Shiraz University of Medical Sciences. Funding: Shiraz University of Medical Sciences, Grant No. 7696. Competing interests: None declared.

Prévalence de la non-notification des erreurs médicales en milieu hospitalier en République islamique d’Iran Résumé Contexte : Les erreurs médicales sont fréquentes dans les établissements de soins, ce qui a pour effet de mettre en péril la sécurité des patients et d’augmenter les coûts associés. Objectifs : La présente étude transversale avait pour objectif d’examiner les taux et les raisons de la non‐notification des erreurs médicales à l’hôpital de Nemazee, à Chiraz en République islamique d’Iran. Méthodes : Des questionnaires auto‐administrés ont été remplis par 283 membres du personnel, parmi lesquels des médecins, des membres du personnel infirmier et des étudiants en médecine. Une analyse de variance à sens unique, le test post hoc de la différence la moins significative de Fisher, le coefficient de corrélation de Spearman et les tests de corrélation intraclasse ont été utilisés pour les analyses statistiques. Résultats : La quasi-totalité des participants (95,8 %) avait observé au moins une erreur médicale au cours de l’année précédente, plus de la moitié (50,5 %) ayant relevé entre 3 et 10 erreurs. Pour signaler les erreurs médicales, les médecins et les étudiants en médecine privilégiaient la méthode verbale et informelle (40,3 % et 41,8 % respectivement), tandis que le personnel infirmier préférait les formulaires écrits (45,7 %). Les résultats indiquent des différences significatives entre les groupes concernant les obstacles individuels et organisationnels en général, et entre toutes les sous-catégories (p < 0,001). Conclusion : L’étude a montré que la complexité juridique et les problèmes de confidentialité constituaient les principaux obstacles à la notification des erreurs médicales.

معدل انتشار عدم اإلبالغ عن األخطاء الطبية يف املستشفيات يف مجهورية إيران اإلسالمية مهرداد أسكريان، سيد رشافت، مريم قديس، زهرة شايان، تشارلز بالينيك، ناهيد حاتم، يافور إنشيف اخلالصة اخللفية: ًكثريا ما تقع األخطاء الطبية يف مرافق الرعاية الصحية، مما ُي ِّعرض سالمة املرىض للخطر، ويزيد من التكاليف املرتبطة بذلك. األهداف: هدفهذا االستقصاء املقطعي إىل بحث معدالت عدم اإلبالغ عن األخطاء الطبية يف مستشفى نامزي يف مدينة شرياز بجمهورية إيران اإلسالمية، وأسباب ذلك. طرق البحث: استكمل 283 ً موظفااالستبيانات ً، منذاتيا بينهم أطباء وممرضات أو ممرضون وطالب يف الكليات الطبية. ُواست ِخدم التحليل أحادي االجتاه للفروق، واختبار فيرش َالبعدي ألقل فرق معنوي، واختبار معامل سبريمان للرتابط، واختبار معامل الرتابط داخل الفئة، ألغراض التحليالت اإلحصائية. النتائج: الحظ مجيع املشاركني ًتقريبا )95.8%( ًخطأ ًطبيا ًواحدا عىل األقل خالل العام السابق، والحظ أكثر من نصفهم )50.5%( حدوث 3-10 أخطاء. وكانت الطريقة ُامل َّفضلة لدى األطباء وطالب الكليات الطبية لإلبالغ عن األخطاء الطبية هي الطريقة الشفوية وغري الرسمية )40.3% و41.8% عىل التوايل(، يف حني َّ ل فضاملمرضون واملمرضات َالنامذج املكتوبة ) %(. 45.7وأشارت النتائج إىل وجود اختالفات كبرية بني املجموعات فيام يتعلق باحلواجز الفردية والتنظيمية ٍ بصفةعامة، وبني مجيع الفئات الفرعية )P<0.001(. االستنتاجات: ُثبتأن الشواغل املتعلقة بالتشابكات القانونية وقضايا الرسية هي العقبات الرئيسية التي تعرتض اإلبالغ عن األخطاء الطبية.

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Assessment of nurses’ patient safety culture in 30 primary health-care centres in Tunisia

Mohamed Ayoub Tlili,1,2 Wiem Aouicha,1 Mohamed Ben Dhiab3 and Manel Mallouli4

1Laboratoire de Recherche LR12ES03, Faculté de Médecine de Sousse, Université de Sousse, Sousse, Tunisia (Correspondence to: Mohamed Ayoub Tlili: [email protected]). 2Ecole Supérieure des Sciences et Techniques de la Santé de Sousse, Université de Sousse, Sousse, Tunisia. 3Vice-Dean, Faculté de Médecine de Sousse, Université de Sousse, Sousse, Tunisia. 4Département de Médecine Familiale et Communautaire, Laboratoire de Recherche LR12ES03, Faculté de Médecine de Sousse, Université de Sousse, Sousse, Tunisia

Abstract Background: Ensuring patient safety and health-care quality remain priorities and challenges worldwide and the role of nurses is essential to meet these challenges. Developing patient safety culture is a key component to improve patient safety and health-care quality. Aims: To assess nurses’ patient safety culture in primary health-care centres in Tunisia and to determine its associated factors. Methods: This was a multicentre, cross-sectional descriptive study conducted across 30 primary health-care centres in Tunisia, using the French validated version of the Hospital Survey on Patient Safety Culture questionnaire. All the nurses working in these centres were invited to participate in the study (n = 158). Results: The response rate for participation in the study was 87.3%. The dimension of “teamwork within units” had the highest score (70.6%). Three safety dimensions had low scores: “frequency of event reporting” (27.6%), “staffing” (34.76%) and “nonpunitive response to errors” (36.5%). Two factors were associated with patient safety culture: participation in risk management committees, and district of the primary care centre. Conclusions: The level of nurses’ patient safety culture needs to be improved in primary health-care centres in Tunisia. Strategies to nurture patient safety culture should focus upon building leadership capacity that supports open communication, blame-free environment, teamwork and continuous organizational learning. Keywords: Patient safety culture, nurses, patient safety, public health, primary care Citation: Tlili MA; Aouicha W; Ben Dhiab M; Mallouli M. Assessment of nurses’ patient safety culture in 30 primary health-care centres in Tunisia. East Mediterr Health J. 2020;26(11):1347-1354. https://doi.org/10.26719/emhj.20.026 Received: 12/06/19; 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 hospitals for treatment and specialized diagnosis. The third level of care provides specialized consultative care, Adverse events (AEs) remain a global challenge, and usually on referral from primary and secondary care, millions of people are prone to death or injury due to along with teaching and research functions. preventable medical errors (1) and several studies have Primary healthcare centres provide the first contact shown the severity of these AEs in terms of cost, frequen- for patients and quality and patient safety in these cy and serious consequences (2). As a result, enhancing facilities are vital (1,5). However, since severe and patient safety has become a priority for healthcare sys- complicated cases requiring special treatment are tems and providers (2). handled in hospitals, both healthcare providers and local The situation is more difficult and serious in communities tend to underestimate the importance developing countries with a higher risk of patient harm of primary healthcare services (1). In fact, it has been due to the limitation of resources and lack of adequate identified that a significant proportion of safety incidents infrastructure. In Tunisia, a study in the town of Sousse arising in hospitals originate at the earlier levels of care showed that the rate of AEs varied between 10% and 11.3% (5), and some errors in primary care can result in severe (3). The rates of AEs vary according to the sectors, the consequences (1,6,7). A study in Spain deemed that 64.3% nature of the services and levels of care, depending on of AEs in primary care were preventable (8). the specific countries (4). Health care in Tunisia is divided To prevent such harm, there is a growing recognition into public and private structures. The public structures of the importance of establishing a patient safety culture are organized on 3 levels of care. The front-line (first-line) (PSC) (2,9–12). PSC is defined as the product of individual structures include primary healthcare centres serving the and group values, attitudes, perceptions, competencies community with primary and essential care. The second- and patterns of behaviour that determine commitment level structures (regional hospitals) refer to a second tier to the style and proficiency of an organization’s safety of the healthcare system, in which patients from primary management (13). Furthermore, it should be noted health care are referred to specialists in higher-level that development of PSC starts with evaluation of its

1347 Research article EMHJ – Vol. 26 No. 11 – 2020 existing level (1,14). In particular, nurses as healthcare Cronbach a was 0.88 for the whole questionnaire and providers believe that patient safety is primarily a varied between 0.46 and 0.84 for the individual dimen- nursing responsibility (14,15), and it has been estimated sions (20). that > 90% of potential medication errors are discovered Ten PSC dimensions were explored by the French by nurses (14). Thus, nurses are considered key to safety version through 45 items. The questionnaire user’s improvement and play a vital role in enhancing quality of care (12,14,16). The nature of work carried out by guide defined and described the 10 dimensions related nurses and the roles they perform provide them with to PSC as follows (19). (D1) Overall perceptions of patient opportunities to reduce AEs and intercept healthcare safety: procedures and systems are good at preventing errors before they occur (12). Thus, assessment of nurses’ errors and there is a lack of patient safety problems. PSC is crucial to identify the strengths and weaknesses of (D2) Frequency of events reported: mistakes of the their safety culture and to help units’ caregivers identify following types are reported: (1) mistakes caught and the patient safety problems that they have. corrected before affecting the patient; (2) mistakes with It has been shown that the level of PSC in Tunisia is low no potential to harm the patient; and (3) mistakes that (10,17,18). This can be explained by the lack of professional could harm the patient but do not. (D3) Supervisor/ involvement in training sessions on patient safety and manager expectations: supervisors/managers consider the late introduction of the concept of PSC in Tunisia. For staff suggestions for actions promoting and improving example, a study in Tunisian operating rooms showed patient safety; praising staff for following patient safety that all dimensions of PSC needed improvement (10). procedures; and do not overlook patient safety problems. Another study showed that no dimension was considered (D4) Organizational learning – continuous improvement: as developed (17). To our knowledge, no studies have assessed nurses’ PSC in Tunisia, specifically in crucial mistakes have led to positive changes and changes are frontline healthcare facilities that deliver essential care. evaluated for effectiveness. (D5) Teamwork within units: Therefore, we assessed nurses’ PSC in Tunisian primary staff support each other, treat each other with respect, healthcare centres and determined its associated factors. and work together as a team. (D6) Communication openness: staff freely speak up if they see something that Methods may negatively affect a patient and feel free to question those with more authority. (D7) Nonpunitive response to Study design, setting, duration and errors: staff feel that their mistakes and event reports are participants not held against them and that mistakes are not kept in This was a cross-sectional multicentre study from Janu- their personnel file. (D8) Staffing: there are enough staff ary to April 2016 in all 30 primary healthcare centres in to handle the workload, which is appropriate to provide Sousse, Kasserine and Kairouan, Tunisia. These centres the best care for patients. (D9) Management support for are partners of the Faculty of Medicine of University of patient safety: hospital management provides a work Sousse and carry out consultations 4 days a week. Each climate that promotes patient safety and shows that centre has 1 or 2 doctors and an average of 4 nurses. patient safety is a top priority. (D10) Teamwork across All 158 nurses involved in the selected primary units: hospital units cooperate and coordinate with one healthcare centres were invited to participate in the another to provide the best care for patients. study and 138 provided survey feedback. Nurses were The questionnaire assesses 10 dimensions deemed divided into registered nurses and specialized nurses related to PSC in a way that if the professionals have a with specific additional training for particular specialties dysfunction in one or more dimensions (score < 50%) it (emergency, paediatric and geriatric care). Nurses who were not involved in healthcare practices and those with reflects a failing PSC. For example, if professionals work < 1 month’s experience were excluded. This exclusion in a punitive environment (D7) or have dysfunctional criterion was recommended by the questionnaire’s user teamwork (D5), it means PSC is failing. To have a well- guide provided by the Coordination Committee of the developed PSC, the 10 dimensions must be developed Clinical Evaluation and Quality in Aquitaine (CCECQA), (score > 75%) (19). which was responsible for validation of the French The survey also explored nurses’ perception of patient version of the questionnaire (19). safety quality (1 item), and the number of AEs reported Questionnaire during the last 12 months (1 item), which referred to the number of events that the nurses responding to the survey The current study used the French version of the Hospi- reported. The questionnaire also included a section on tal Survey on Patients Safety Culture (HSOPSC) questionnaire, which was translated and validated by the CCCEQA general information on the participants, which was used (20). It is the most broadly used instrument to evaluate to determine the factors associated with PSCeus, namely: PSC because of its favourable psychometric properties; it professional title (specialty), sex, age, work experience, is a valid and reliable instrument that allows the study participation in risk management committees, and concept (PSC) to be measured appropriately (21). The district of the primary healthcare centre.

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A Likert scale of 5 points was used to explore Table 1 Characteristics of participants participants’ PSC perception ranging from ‘strongly Characteristics n % disagree’ to ‘strongly agree’ or from ‘never’ to ‘always’ Professional title/specialty depending on the nature of the item. Specialized nurses 46 33.3 Data collection and ethical considerations Registered nurses 92 67.7 After obtaining institutional ethics committee approval Total 138 100 and administrative authorization from different centres’ Sex management, a self-reported paper-based questionnaire Female 102 73.9 was distributed to the participants. The investigator went Male 36 26.1 to the centre and distributed the questionnaire after ex- Total 138 100 plaining the aims and outcomes of the study to all the Age nurses meeting the inclusion criteria and who agreed > 40 years 90 65.2 to respond. They could freely and anonymously fill in ≤ 40 years 48 34.8 the questionnaire and return their responses directly to Total 138 100 the investigator. The investigators did not work in the Work experience centres and only went to distribute the questionnaires. < 10 years 35 25.4 The data entry and analysis were confided to another re- ≥ 10 years 103 74.6 searcher. Total 138 100 Data analysis Participation in risk management committees Data analysis was performed using SPSS version 20 Yes 24 17.4 and Epi info 6.04d for Windows. Descriptive statistical No 114 82.6 analysis such as frequencies and percentages of positive Total 138 100 responses for each item and dimension were used to ex- Location of primary healthcare centre amine professionals’ perceptions about PSC. Items were Urban 102 73.9 worded in both positive and negative terms. For items Rural 36 26.1 with a positive formulation, answers “strongly agree/ agree” or “most of the time/always” were considered pos- Nurses’ perception of patient safety quality and itive. For items with a negative formulation, the answers “strongly disagree/disagree” or “never/rarely” responses frequency of reported AEs were considered positive for PSC. Nurses’ perception of patient safety quality in the prima- Items with negative formulation were identified ry healthcare centres was ranked as acceptable in 57.2% according to the questionnaire’s user guide (19) and of cases and poor in 17.4% (Table 2). Ninety-eight (71%) of the participants declared that they did not report any AE were coded conversely. According to the user guide, if in the last 12 months. none of the dimensions’ sections was entirely filled, the questionnaire would not be taken into account (19). PSC dimensions Also, if fewer than half of the items in the questionnaire Overall perception of patient safety had an average pos- were completed, or the same answers were given to all itive score of 53.65% (Table 3). The percentage of positive the items, the questionnaire was considered ineligible and excluded (19). A bivariate analysis was carried out to highlight the associations between the sociodemographic Table 2 Nurses perception of patient safety quality and and professional data and the different dimensions of number of reported adverse events during the last 12 months PSC. Percentages were compared by Pearson’s χ2 test. The Nurses perception of patient safety quality n % materiality threshold was set at 0.05. Excellent 9 6.5 Very good 25 18.2 Results Acceptable 79 57.2 Poor 24 17.4 Participant characteristics Failing 1 0.7 A total of 138 participants provided survey feedback No. of events reported n % and the response rate was 87.3%; 92 (67.7%) were reg- None 98 71 istered nurses and 46 (33.3%) were specialized nurses 1 or 2 20 14.5 (Table 1). Most respondents (n = 102; 73.9%) were female, 3–5 8 5.8 and the male:female ratio was 0.35. One hundred and 6–20 5 3.6 three (74.6%) nurses had work experience of > 10 years. > 20 7 5.1

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Table 3 Scores and items of the 10 dimensions of patient safety culture Items of patient safety culture dimensions Absolute Average positive frequency (n) response (%) D1: Overall perceptions of safety 53.65 Patient safety is never sacrificed to get more work done 90 65 Our procedures and systems are good at preventing errors from happening 83 59.8 It is just by chance that more serious mistakes do not happen around here 67 48.9 We have patient safety problems in this facility 56 40.9 D2: Frequency of events reported 27.7 When a mistake is made, but is caught and corrected before affecting the patient, it is reported 40 29.2 When a mistake is made, but has no potential to harm the patient, it is reported 33 24 When a mistake is made that could harm the patient, but does not, it is reported 41 29.9 D3: Supervisor/manager expectations and actions promoting patient safety 53.47 Manager says a good word when he/she sees a job done according to established patient safety procedures 85 61.3 Manager seriously considers staff suggestions for improving patient safety 74 53.3 Whenever pressure builds up, my manager wants us to work faster, even if it means taking shortcuts 71 51.1 My manager overlooks patient safety problems that happen over and over 67 48.2 D4: Organizational learning and continuous improvement 48.66 We are actively doing things to improve patient safety 94 67.9 Mistakes have led to positive changes here 77 55.5 After we make changes to improve patient safety, we evaluate their effectiveness 106 76.6 We are given feedback about changes put into place based on event reports 14 10.2 We are informed about errors that happen in the facility 47 34.3 In this facility, we discuss ways to prevent errors from happening again 66 47.5 D5: Teamwork within units 70.6 People support one another in this facility 93 67.1 When a lot of work needs to be done quickly, we work together as a team to get the work done 109 78.8 In facility, people treat each other with respect 95 68.6 When one area in this unit gets really busy, others help out 94 67.9 D6: Communication openness 42.13 Staff will freely speak up if they see something that may negatively affect patient care 70 50.4 Staff feel free to question the decisions or actions of those with more authority 39 28.5 Staff are afraid to ask questions when something does not seem right 66 47.5 D7: Nonpunitive response to error 36.5 Staff feel like their mistakes are held against them 49 35.8 When an event is reported, it feels like the person is being written up, not the problem 56 40.9 Staff worry that mistakes they make are kept in their personnel file 45 32.8 D8: Staffing 34.76 We have enough staff to handle the workload 67 48.9 Staff in this facility work longer hours than is best for patient care 22 16 We work in crisis mode trying to do too much, too quickly 54 39.4 D9: Management support for patient safety 51.07 Management provides a work climate that promotes patient safety 60 43.8 The actions of management show that patient safety is a top priority 79 56.9 Management seems interested in patient safety only after an adverse event happens 58 42.3 Units work well together to provide the best care for patients 85 61.3

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Table 3 Scores and items of the 10 dimensions of patient safety culture (Concluded) Items of patient safety culture dimensions Absolute Average positive frequency (n) response (%) D10: Teamwork across units 45.95 There is good cooperation among units that need to work together 75 54.7 Units do not coordinate well with each other 55 40.1 It is often unpleasant to work with staff from other units 55 40.1 Things “fall between the cracks” when transferring patients from one unit to another 53 38.7 Important patient care information is often lost during shift changes 83 59.8 Problems often occur in the exchange of information across units 58 42.3

responses was highest for teamwork within units (70.6%). to previous studies (1,25,27). However, when it came The lowest scores were for frequency of event reporting to critical care areas such as operating rooms (10) and (27.7%), staffing (34.76%) and nonpunitive response to er- intensive care units (28), this dimension had a low score ror (36.5%). (41.7% and 46.99%, respectively). This may be due to the fact that primary healthcare centres are small buildings Factors associated with PSC with fewer staff compared to hospitals and critical The dimensions of PSC were not significantly associat- care units and are unsophisticated environments that ed with sex, professional title, or work experience. Two encourage teamwork (29). factors were associated with PSC dimensions: frequency Staffing had a positive score of 34.76%, and most of AEs reported was significantly higher among partic- nurses reported that they did not have enough staff P ipants involved in risk management committees ( = to handle the workload, and that they worked longer 0.02); and overall perception of safety was significantly hours than are best for patient care. This situation may higher among nurses working in urban compared with have severe negative consequences for patient safety rural districts (P = 0.03). and quality of care. O’Brien-Pallas et al. investigated the relationship between nurse staffing, workload and Discussion patient outcomes. They found that nurse staffing (fewer To our knowledge, there have been no studies of PSC registered nurses), increased workload, and an unstable among nurses working in primary healthcare in Tuni- nursing environment was linked to negative patient sia. Therefore, the present study was conducted to as- outcomes, including falls and medication errors (30). sess nurses’ PSC in Tunisian primary healthcare centres. They also reported that when nursing demand/supply The dimension of teamwork within units had the highest levels exceeded 80%, negative outcomes increased for score (70.6%). Three dimensions had low scores, namely, nurses themselves and hospitals, as well as patients. frequency of event reporting (27.6%), staffing (34.76%) The dimension that had the lowest score was and nonpunitive response to errors (36.5%). Two factors frequency of events reported (27.7%). This under-reporting were associated with PSC: participation in risk manage- can be explained by the fact that the commission of error ment committees, and district of the primary care centre. is always considered to indicate lack of skill and rarely Recently, patient safety in primary care has been given seen as a learning opportunity. Several barriers exist to increasing attention (22), and many studies have shown reporting AEs, including insufficient time to report, lack a high level of AEs with negative consequences (1,6,7,23). of feedback, fear of blame and damage to reputation in a Given the importance of assessing PSC to enhance patient competitive environment, and loss of patient confidence safety in primary care, several studies have sought to (11,31). This dimension was similar to nonpunitive determine professionals’ PSC in this setting (1,5,9,24–26). response to error, which also had a low score (36.5%). Many studies have focused on nurses, in the belief that Nurses reported that they felt that their mistakes were understanding nurses’ perceptions are crucial for policy- held against them and their involvement in the AE was makers to address PSC in relation to nurses’ staffing being highlighted rather than the AE itself. This problem policies (12,14,15). The dimension of overall perception of of under-reporting AEs must be taken into consideration safety had a score of 53.65%. This reflects the lack of safety and treated with vigilance; nurses should be encouraged standards in the primary healthcare centres and the need to report AEs and even rewarded for so doing. It is to implement corrective measures to increase awareness essential to establish a culture in which individuals are of this issue among professionals. Indeed, 59.1% of nurses supported to identify and report AEs without threat of confirmed that they had problems with security in their punitive action or blame. Reporting of AEs is an integral workplace. part of a continuous cycle of improving patient safety We found that the dimension of teamwork within and quality of care that includes error identification, units had the highest score (70.6%) and this was similar reporting, analysis and corrective actions (32).

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In our study, participants who were engaged in risk of an anonymous reporting system that protects the management committees had a significantly higher score reporter is therefore recommended. for the dimension frequency of events reported (37.2% Our study had some limitations. First, assessment of vs 17.7%; P = 0.02). This finding agrees with results from PSC using a self-administered questionnaire could have the PSC survey that was conducted in operating rooms been associated with declaration bias. A self-administered in Tunisia (10). Risk management describes a dynamic questionnaire may influence the responses of those process that includes all measures for systematic who, for fear of reprisal or prosecution, give desirable identification, analysis, assessment, surveillance and answers that do not reflect reality. Second, HSOPSC did control of risks. An effective risk management should not not allow us to calculate an overall score for PSC for all start only after the evaluation of an incident but when the targeted centres, which would have allowed rapid failure can still be avoided and damage can be prevented. comparison of quality of care and safety culture between healthcare organizations. By following the questionnaire Overall perception of safety was significantly more guidelines, we were only able to calculate a score for each developed among nurses working in urban than in rural dimension without calculating a mean score for all the areas (60.1% vs 40.2%; P = 0.03). This difference can be dimensions combined. Third, there was possible recall explained by the fact that, in Tunisia, urban healthcare bias, specifically when remembering the number of AEs institutions are better equipped with more sophisticated reported, resulting in possible under- or overestimation equipment and better human and material resources. of reported results. Finally, even though we included all We recommend systematic improvement of staff the training centres of the targeted region, the sampling qualifications by providing training opportunities technique did not allow us to assume that these included and educational interventions to promote better settings were representative of the entire primary understanding of the principles of teamwork, help staff healthcare system in Tunisia. acknowledge each other’s roles and perspectives, and develop effective communication strategies. At the level Conclusions of practice, policy-making, administration, research Our findings demonstrated that none of the PSC dimen- and curriculum, we recommend improved training of sions were developed in our primary healthcare centres. nurses regarding patient safety. To this end, the World We highlighted different areas of concern, such as fre- Health Organization has published 2 guides: the first quency of events reported, nonpunitive response to er- is for students, to be integrated into health universities ror, and staffing. More attention should be paid to PSC (Patient Safety Curriculum Guide for Medical Schools) in primary healthcare because changing values and atti- (33); and the second is designed for health professionals as tudes needs time and motivation through training and part of continuing education (Patient Safety Curriculum improving risk management skills among nurses. Also, Guide Multi-professional Edition) (34). Improvement the results highlight the necessity of implementation of quality of care and patient safety by implementing of quality management systems in Tunisian primary a quality management system is essential, with healthcare centres. Strategies to nurture PSC should fo- managerial training concerning communication and cus upon building leadership capacity that supports open nursing leadership. Nurses need to feel protected and communication, blame-free environment, teamwork and encouraged to report errors and AEs, and introduction continuous organizational learning.

Acknowledgement We thank the professionals in all the centres where the study was conducted for their cooperation and the supportive working conditions that they offered. Funding: None. Competing interests: None declared.

Évaluation de la culture de la sécurité des patients chez le personnel infirmier dans 30 centres de soins de santé primaires en Tunisie Résumé Contexte : Garantir la sécurité des patients et la qualité des soins de santé demeure une priorité et un défi dans le monde entier face auxquels le personnel infirmier joue un rôle essentiel. Le développement de la culture de la sécurité des patients constitue un élément clé pour améliorer la sécurité de ces derniers ainsi que la qualité des soins de santé. Objectifs : Évaluer la culture de la sécurité des patients chez le personnel infirmier dans les centres de soins de santé primaires tunisiens et déterminer les facteurs qui y sont associés.

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Méthodes : Il s’agissait d’une étude descriptive transversale multicentrique menée dans 30 centres de soins de santé primaire tunisiens à l’aide de la version française validée du questionnaire de l’enquête hospitalière sur la culture de la sécurité des patients. L’ ensemble du personnel infirmier travaillant dans ces centres a été invité à participer à l’étude (n = 158). Résultats : Le taux de réponse concernant la participation à l’étude a été de 87,3 %. La dimension « travail d’équipe au sein des unités » a obtenu le score le plus élevé (70,6 %). Trois dimensions de la sécurité présentaient des scores faibles : « fréquence de notification des événements » (27,6 %), « dotation en personnel » (34,76 %) et « réponse non punitive à l’erreur » (36,5 %). Deux facteurs étaient associés à la culture de la sécurité des patients : la participation aux comités de gestion des risques et le district du centre de soins primaires. Conclusions : Le niveau de culture de la sécurité des patients chez le personnel infirmier doit être amélioré dans les centres de soins de santé primaires en Tunisie. Les stratégies visant à développer la culture de la sécurité des patients doivent porter sur le renforcement des capacités d’encadrement qui favorisent une communication ouverte, un environnement professionnel bienveillant, le travail d’équipe et un apprentissage organisationnel continu.

تقييم ثقافة سالمة املرىض لدى طواقم التمريض يف 30 ً مركزامن مراكز الرعاية الصحية َّاألولية يف تونس حممد أيوب تلييل، وئام عويشة، حممد بن ذياب، منال ملويل اخلالصة اخللفية: اليزال ضامن سالمة املرىض وجودة الرعاية الصحية من األولويات والتحديات التي تواجه قطاع الصحة يف مجيع أنحاء العامل، وال غنى عن َد ْور طواقم التمريض للتغلب عىل هذه التحديات. ُوي َعد نرش ثقافة سالمة املرىض ًعنرصا ًأساسيا لتحسني سالمة املرىض وجودة الرعاية الصحية. األهداف: هدفتهذه الدراسة إىل تقييم ثقافة سالمة املرىض لدى طواقم التمريض يف مراكز الرعاية الصحية َّاألولية يف تونس، وحتديد العوامل املرتبطة هبا. طرق البحث: كانت هذه دراسة وصفية مقطعية متعددة املراكز ُأجريت عىل 30 ً مركزامن مراكز الرعاية الصحية َّاألولية يف تونس، باستخدام النسخة الفرنسية ُاملجازة من َم ْسح املستشفيات من خالل استبيان ثقافة سالمة املرىض. ُعي ودمجيع أفراد طاقم التمريض العاملني يف هذه املراكز للمشاركة يف الدراسة )العدد = 158(. النتائج: بلغ معدل االستجابة للمشاركة يف الدراسة 87.3%. َّوحقق ُعد ب»العمل اجلامعي داخل الوحدات« أعىل الدرجات )70.6%(. وحصلت ثالثة أبعاد متعلقة بالسالمة عىل درجات منخفضة، وهي: »تواتر اإلبالغ عن األحداث« )27.6%(، و«التوظيف« )34.76%(، و«االستجابة غري العقابية لألخطاء« )36.5%(. وارتبط عامالن بثقافة سالمة املرىض: املشاركة يف جلان إدارة املخاطر، واملنطقة التي يقع فيها مركز الرعاية األولية. االستنتاجات: َث َّمةحاجة إىل حتسني مستوى ثقافة سالمة املرىض لدى طواقم التمريض يف مراكز الرعاية الصحية َّاألولية يف تونس. وينبغي أن ِّتركز اسرتاتيجيات تعزيز ثقافة سالمة املرىض عىل بناء القدرات القيادية التي تدعم التواصل ُاملنفتح، وهتيئة بيئة خالية من إلقاء اللوم، والعمل اجلامعي، ُّوالتعلم التنظيمي املستمر.

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Hospital survey on patient safety culture (HSOPS): variabili- ty of scoring strategies. Int J Qual Health Care 2017 Oct;29(5):685–92. https://doi.org/10.1093/intqhc/mzx086 22. Verbakel NJ, Zwart DL, Langelaan M, Verheij TJ, Wagner C. Measuring safety culture in Dutch primary care: psychometric characteristics of the SCOPE-PC questionnaire. BMC Health Serv Res 2013;13:Article number 354. https://doi.org/10.1186/1472- 6963-13-354 23. Sandars J, Esmail A. The frequency and nature of medical error in primary care: understanding the diversity across studies. Fam Pract 2003 Jun;20(3):231–6. https://doi.org/10.1093/fampra/cmg301 24. Smits M, Christiaans-Dingelhoff I, Wagner C, Wal G van der, Groenewegen PP. The psychometric properties of the “Hos- pital Survey on Patient Safety Culture” in Dutch hospitals. BMC Health Serv Res 2008;8: Article number 230. https://doi. org/10.1186/1472-6963-8-230 25. Mohamed AM, Ali MS, Gewaifel GI. Assessment of Patient Safety Culture in Primary Healthcare Services in Alexandria, Egypt. Glob J Epidemiol Public Health 2015;2:5–14. http://dx.doi.org/10.12974/2313-0946.2015.02.01.1 26. Tabrizchi N, Sedaghat M. The frst study of patient safety culture in Iranian primary health centers. Acta Med Iran 2012;50(7):505–10. PMID:22930384 27. Ghobashi MM, El-ragehy HAG, Ibrahim HM, Al-Doseri FA. Assessment of patient safety culture in primary health care settings in Kuwait. Epidemiol Biostat Public Health 2014;11(3). https://doi.org/10.2427/9101 28. Minuzzi AP, Salum NC, Locks MOH. Avaliação da cultura de segurança do paciente em terapia intensiva na perspectiva da equi- pe de saúde. Texto Contexto Enferm 2016;25(2) (in Portuguese). https://doi.org/10.1590/0104-07072016001610015 29. Wilson T, Pringle M, Sheikh A. Promoting patient safety in primary care. BMJ 2001 Sep 15;323(7313):583–4. http://dx.doi. org/10.1136/bmj.323.7313.583 PMID:11557689 30. Duffeld C, Diers D, O’Brien-Pallas L, Aisbett C, Roche M, King M, et al. Nursing staffng, nursing workload, the work environment and patient outcomes. Appl Nurs Res. 2011 Nov;24(4):244–55. https://doi.org/10.1016/j.apnr.2009.12.004 31. Rea D, Griffths S. Patient safety in primary care: incident reporting and signifcant event reviews in British general practice. Health Soc Care Community 2016 Jul;24(4):411–9. https://doi.org/10.1111/hsc.12221 32. Cooke DL, Dunscombe PB, Lee RC. Using a survey of incident reporting and learning practices to improve organisational learning at a cancer care centre. BMJ Qual Saf. 2007;16:342–8. https://doi.org/10.1136/qshc.2006.018754 33. Patient safety curriculum guide for medical schools 2009. Geneva: World Health Organization; 2009 (https://apps.who.int/iris/ bitstream/handle/10665/44091/9789241598316_eng.pdf?sequence=1&isAllowed=y, accessed 25 April 2020). 34. Patient safety curriculum guide: multi-professional edition. 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Travel burden and geographic access to health care among children with cancer in Saudi Arabia

Abdulrahman Alsultan,1,2 Abdullah Aljefri,3 Mouhab Ayas,3 Musa Alharbi,4 Nawaf Alkhayat,5 Faisal Al-Anzi,6 Fawwaz Yassin,7 Fawaz Alkasim,8 Qasim Alharbi,9 Shaker Abdullah,10 Mohammed Abrar10 and Wasil Jastaniah10,11

1Department of Pediatrics, College of Medicine, King Saud University, Riyadh, Saudi Arabia (Correspondence to: A. Alsultan: [email protected]). 2Department of Pediatric Hematology/Oncology, King Abdullah Specialist Children’s Hospital, Riyadh, Saudi Arabia. 3Department of Pediatric Hematol- ogy/Oncology, King Faisal Specialist Hospital & Research Center, Riyadh, Saudi Arabia. 4Department of Pediatric Hematology/Oncology, Cancer Center, King Fahad Medical City, Riyadh, Saudi Arabia. 5Department of Pediatrics, Prince Sultan Military Medical City, Riyadh, Saudi Arabia. 6Prince Faisal Bin Bandar Cancer Center, Qassim, Saudi Arabia. 7Department of Pediatric Hematology/Oncology, King Faisal Specialist Hospital & Research Center, Jeddah, Saudi Arabia. 8Department of Pediatric Hematology and Oncology, King Saud Medical City, Riyadh, Saudi Arabia. 9Department of Pediatric Hematology/Oncology, King Fahad Specialist Hospital, Dammam, Saudi Arabia. 10Department of Oncology, Princess Noorah Oncology Center, King Saud Bin Abdulaziz University and King Abdulaziz Medical City, Jeddah, Saudi Arabia. 11Department of Pediatrics, Faculty of Medicine, Umm Al-Qura University, Makkah, Saudi Arabia.

Abstract Background: Travel burden has a substantial psychosocial impact and financial strain on childhood cancer patients and their families. Aims: To study the geographic distribution of childhood cancer and assess the travel burden for care in Saudi Arabia. Methods: This was a cross-sectional multi-institutional study that enrolled 1657 children with cancer who were diagnosed between 2011 and 2014. Cancer type/stage, city/region of residence, and city/region of treating centre were recorded. Travel burden was measured based on a 1-way distance in kilometres from the city centre to the treatment institution. This study was supported by Sanad Children’s Cancer Support Association. Results: Diagnosis was leukaemia (45.2%), non-CNS solid tumours (30.2%), lymphoma (12.3%), CNS tumours (11.8%) and histiocytosis (0.5%). Childhood cancer centres were in the same city as where the patients lived in 652 (39.3%) cases, same region but different city in 308 (18.6%), different regions in 613 (37%), and not known in 84 (5.1%). The mean 1-way travel distance for patients who lived in different regions was 790 (range, 116–1542) km. A total of 536 (32%) patients lived ≥ 400 km and 216 (13%) > 1000 km from the treatment centre. Among 642 patients with acute lymphoblastic leukaemia who required 2–3 years of therapy, 197 (31%) lived ≥ 400 km and 94 (15%) >1000 km from the treatment centre. Conclusions: Nearly two thirds of patients with childhood cancer lived in different cities than the treatment centres, including one third of patients who lived ≥ 400 km away. There is a need to develop strategies to improve access to childhood cancer care. Keywords: cancer, geographic distribution, paediatrics, Saudi Arabia, travel burden Citation: Alsultan A; Aljefri A; Ayas M; Alharbi M; Alkhayat N; Al-Anzi F; et al. Travel burden and geographic access to health care among children with cancer in Saudi Arabia. East Mediterr Health J. 2020;26(11):1355-1362. https://doi.org/10.26719/emhj.20.020 Received: 10/04/19; accepted: 13/11/19 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 Childhood cancer in Saudi Arabia affects 1 in 10 000 children. The 2015 Saudi Cancer Registry Report showed The outcome of childhood cancer has improved signif- that leukaemia was the most common childhood icantly in recent decades with current estimated 5-year cancer (35%) followed by brain tumours (12.2%) and survival rates of 80%. This progress has been due to suc- non-Hodgkin’s lymphoma (12.2%) (5). Centres that treat cessful clinical trials conducted by collaborative research childhood cancer are mainly in 4 (Riyadh, Makkah, groups, such as the Children’s Oncology Group, com- Eastern and Qassim) out of the 13 regions in Saudi bined with advances in supportive care (1,2). However, during progression to cure, other concerns might arise Arabia. Patients and their families in the remaining 9 in families of children with cancer, such as employment regions need to travel long distances by land or air for disruption, high out-of-pocket spending, travel burden, their initial diagnosis and treatment. Increased travel and psychosocial difficulties (3,4). These concerns are distance between the residence of patients and the infrequently addressed in depth with families given that treatment centre is associated with increased financial the focus of medical teams is primarily on delivering burden, work interruption, and residence relocation (6). optimal treatment. Governmental financial support for In a large study in the United Kingdom of Great Britain patients and their families, active involvement of social and Northern Ireland, travel burden was associated with service teams at cancer centres, and support from non- survival disadvantage among cancer patients (7). profit organizations are ways to address some of these The travel burden and its impact on cancer outcome concerns in Saudi Arabia. have not been studied in Saudi Arabia. In this study,

1355 Research article EMHJ – Vol. 26 No. 11 – 2020 we examined the geographic distribution of childhood our study represented 50% of all childhood cancer cases cancer in different regions in Saudi Arabia, assessed the expected to be diagnosed during the study period, based burden of travel among patients and their families, and on the Saudi Cancer Registry (5). A total of 1501 (91%) pa- evaluated the influence of travel burden on the initial tients were Saudi and the remaining 156 (9%) were from cancer staging in solid tumours. other nationalities. Leukaemia was the most common diagnosis (45.2%), followed by non-CNS solid tumours Methods (30.2%), lymphoma (12.3%), CNS tumours (11.8%) and last- ly histiocytosis (0.5%). There was no marked difference in Patient population the pattern of cancer among regions. Figure 1 shows the proportion of children with cancer in each region as well We performed a cross-sectional multi-institutional study as the proportion of normal children aged ≤ 14 years. The in 10 centres that treat most cases of childhood cancer in proportion of children with cancer who lived in Riyadh Saudi Arabia. Informed consent was obtained from par- Region was 30.8% of all patients enrolled in our study, ents of all participants and the study was approved by while the proportion of normal children who lived in Ri- the institutional review boards in all participating insti- yadh Region was 24.7% of all normal Saudi children (P < tutions. We enrolled 1657 patients: 917 (55%) male and 740 0.0001). (45%) female. aged ≤ 14 years who were diagnosed with cancer between January 2011 and December 2014. We Travel burden and access to cancer care in collected the following information: cancer type, cancer different regions stage, city/region of residence, and city/region of treatment centre. Data were recorded remotely using RED- Treatment institutions were in the same city for only Cap (Research Electronic Data Capture) electronic data 652 (39.3%) patients (Table 2). The treatment centre was capture tools hosted and stored centrally in a secure Mi- in the same region but different city for 308 (18.6%) pa- crosoft SQL database (8). The study was organized by the tients and the average 1-way travel distance among those Saudi Arabian Pediatric Hematology Oncology Society patients was 159 (range, 19–737) km. The remaining 613 (SAPHOS) as part of a study to determine the prevalence (37%) patients lived in different regions from the treat- of hereditary cancer syndromes, as described previously ment centres with a mean 1-way travel distance of 790 (9). It was supported by Sanad Children’s Cancer Support (range, 116–1542) km. A total of 536 (32%) patients lived Association. ≥ 400 km and > 3 hours travel time from the treatment centres. Among those, 216 (13%) patients lived > 1000 km Geographic distribution and travel burden of from the treatment centre. childhood cancer Patients with acute lymphoblastic leukaemia (ALL) Number of patients, sex and characteristics of cancer required prolonged therapy and frequent visits to cancer were described for each region. The proportion of child- centres for several years. There were 642 patients with hood cancer in each region was compared to the pro- ALL in our study: 283 (44%) lived in the same city as the portion of normal children aged ≤ 14 years living in the treatment centre; 103 (16%) lived in the same region but same region, using data from the demographic survey different city; 230 (36%) lived in a different region; and performed in 2016 by the Saudi General Authority of Sta- the address was unknown for 26 (4%). The average travel tistics (10). Travel burden was assessed using Google map distance for ALL patients who lived in different regions based on a 1-way distance in kilometres from the city cen- was 792 (range, 280–1542) km. A total of 197 (31%) ALL tre where the patients lived, to the treatment institution. patients lived ≥ 400 km from the treatment centre, and 94 (15%) of those lived > 1000 km distant. Data analysis Regional referral pattern in childhood cancer Descriptive analyses were presented as mean (standard deviation) values for continuous data and as frequencies Most patients living in Riyadh (99%), Makkah (90%) and for categorical data. A t test was used to compare 2 means Qassim (90%) Regions were treated in the same region. and χ2 or Fisher’s exact test to compare proportions of Nearly half of patients living in the Eastern Region (45%) 2 groups. Patients who lived in the same city as the treat- had to be treated in Riyadh. Childhood cancer centres in ment institution were used as a reference group. P < 0.05 Riyadh were the main referral centres for most regions, was considered to be statistically significant. Stata Statis- except Madinah and Albaha, and centres in Jeddah treat- tical Software Release 12 was used for all analyses (Stat- ed most patients from these 2 regions (Table 3, Figure 2). aCorp LP, College Station, TX, USA). There were 613 patients who lived in different regions than the cancer centres: 453 (74%) were treated in Riyadh, 139 (23%) in Jeddah and 21 (3%) in Qassim. Results Cancer epidemiology in different regions Discussion Cancer classification and geographic distribution of pa- In this study, we described the geographic distribution of tients who were enrolled in the study are summarized in childhood cancer and assessed the travel burden among Table 1. The total number of patients (n =1657) enrolled in our patients and their families. Nearly two thirds of

1356 Research article EMHJ – Vol. 26 No. 11 – 2020 1 7 5 2 2 4 8 71 21 12 61 16 10 53 57 25 25 28 99 69 20 49 68 90 88 115 642 1657 Total 9 (0.5%) 196 (11.8%) 203 (12.3%) 749 (45.2%) 500 (30.2%) 1 1 3 7 2 2 2 2 2 2 6 9 9 4 4 4 8 0 0 0 0 0 0 0 0 0 0 0 31 17 27 26 ND 84 (5.1%) 1 1 1 1 1 2 2 2 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 13 12 border 20 (1.2%) Northern 1 1 1 1 1 2 2 2 2 6 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 11 12 Albaha 23 (1.4%) 1 1 1 1 1 1 1 1 3 2 2 2 2 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 11 12 10 Najran 28 (1.7%) 1 1 1 1 1 1 3 3 3 3 5 5 2 2 6 0 0 0 0 0 0 0 0 0 0 0 0 0 0 12 14 14 Tabuk 39 (2.4%) 1 1 1 1 3 3 3 3 2 2 2 2 2 6 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 14 18 20 Aljouf 44 (2.7%) 1 3 3 7 5 5 2 2 2 2 9 6 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 15 15 10 23 Hail 57 (3.4%) 1 1 1 3 3 3 5 6 6 6 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 12 12 35 27 63 (3.8%) Qassim 1 1 1 1 1 3 7 2 2 2 2 2 Regions (patient’s home) 4 4 8 8 0 0 0 0 0 0 0 0 0 0 0 0 15 15 25 28 Jazan 67 (4.0%) 1 1 1 1 3 7 5 2 2 2 2 9 9 4 4 8 0 0 0 0 0 0 0 0 0 0 0 0 17 52 25 48 Asir 102 (6.2%) 1 1 1 1 1 3 3 3 3 7 7 5 2 2 2 2 2 9 9 9 4 0 0 0 0 0 0 0 18 36 43 40 108 (6.5%) Madinah 1 1 3 3 3 5 5 5 2 2 2 2 9 6 4 4 8 8 0 0 0 0 0 13 14 10 23 22 22 62 42 69 Eastern 175 (10.6%) 1 1 1 1 1 3 3 7 5 2 9 4 8 0 0 0 0 11 13 15 15 16 10 23 25 39 43 24 20 118 110 143 Makkah 336 (20.2%) 1 1 1 3 3 3 2 6 4 4 4 8 0 0 0 11 13 17 19 14 10 32 23 22 22 56 30 20 49 140 263 238 Riyadh 511 (30.8%) Geographic distribution and characteristics of childhood cancer in Saudi Arabia Acute lymphoblastic leukaemia Acute myeloid leukaemia Acute leukaemia, NOS JMML Chronic myeloid leukaemia Myelodysplastic syndrome Wilms’ tumour Retinoblastoma Ewing’s sarcoma/PNET Neuroblastoma Rhabdomyosarcoma Hepatoblastoma Osteosarcoma Renal cell carcinoma Germ cell tumour Thyroid carcinoma Other sarcoma Other carcinoma Other solid tumour Hodgkin’s lymphoma Non-Hodgkin’s lymphoma Medulloblastoma Glioma Ependymoma ATRT Germ cell tumour Other CNS tumour Total Diagnosis Leukaemia Non-CNS solid tumours Lymphoma CNS tumours Histiocytosis Table 1 = atypical teratoid rhabdoid tumour; PNET peripheral neuroectodermal tumour. NOS = not otherwise specified; ND determined; JMML juvenile myelomonocytic leukaemia; ATRT

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Figure 1 Regional distribution of childhood cancer in Saudi Treatment outcome and survival were not assessed Arabia. Proportion of childhood cancer (C) in each region in in our study. Thus, it is possible that patients living in relation to the total number of childhood cancer cases (n = remote areas might have worse outcome due to delay 1657) is shown. Proportion of normal children aged ≤ 14 years (N) in each region in relation to the total number of normal in managing cancer or treatment-related complications children aged ≤ 14 years in Saudi Arabia (n = 7 864 928) is also such as febrile neutropenia. Nevertheless, there is shown. probably a survival advantage for patients traveling to more experienced childhood cancer centres in Saudi Arabia. This is supported by the survival benefit that was observed in the USA among cancer patients receiving treatment at National Cancer Institute (NCI)-designated cancer centres (14). Establishing satellite facilities of the main NCI cancer centres has improved geographic access to high-quality cancer care, with nearly 85% of the American population living within 3 hours of either a parent or satellite facility (15). There are currently limited numbers of satellite facilities that are administered by large childhood cancer centres in Saudi Arabia. Therefore, establishing satellite facilities or affiliated medical centres should be a priority to improve geographic access to cancer care among Saudi patients. In addition, incorporating survival data in the current Saudi Cancer Registry is essential. There is a need to develop strategies to improve patients lived in cities other than the city of the treatment access to cancer care in Saudi Arabia. Formation of centre, including one third of patients who lived in differ- a national referral system to coordinate between ent regions. The average travel burden was 1-way travel different healthcare sectors will facilitate timely access of 790 km for patients living in different regions than to childhood cancer centres. The integration of local the treatment centres. There was a higher proportion of primary care physicians (PCPs) in the care of children childhood cancer patients who lived in Riyadh Region with cancer is essential (16). Paediatric oncologists (30.8%) compared to 24.7% of normal children living in should encourage parents to have local PCPs for their the region. This was probably caused by residence relo- children. Additionally, there is a need to conduct regular cation to Riyadh by some families to be closer to cancer workshops to train local PCPs and other local healthcare providers on various topics in childhood cancer, to enable treatment centres. The government covers the cost of them to recognize cancer at an early stage, refer patients airline tickets for patients and their parents; however, on promptly to cancer centres, and provide appropriate many occasions families need to drive long distances be- management of potential complications (17). It is also cause of fully booked flights. Additionally, the travel burden is exacerbated by the limited accessibility to assigned local primary care physicians that is a common practice in Saudi Arabia. Thus, most of our patients’ health care is Table 2 Travel burden among children with cancer and their families provided at cancer centres. Locations of treatment centre No. of patients (%) Travel burden has multiple negative effects on Same city 652 (39.3%) cancer patients and their families. One study showed Same region but different city 308 (18.6%) that childhood cancer patients living in rural areas were Different region 613 (37.0%) at higher risk of missing more school days, and their < 200 km 3 (0.1%) caregivers missed more work days and spent more out- 200 – < 400 km 74 (4.5%) of-pocket travel expenses compared to urban residents 400 – < 600 km 122 (7.4%) (6). Travel burden was highest for patients living in rural 600 – < 800 km 104 (6.3%) areas in Australia and was associated with significant 800 – < 1000 km 94 (5.7%) financial strains (11). For colon cancer patients in the 1000 – < 1200 km 124 (7.5%) United States of America (USA), increased travel distance 1200 – < 1400 km 89 (5.4%) to cancer centres was associated with advanced stage 1400 – < 1600 km 3 (0.1%) at diagnosis and lower possibility of receiving adjuvant Unknown 84 (5.1%) chemotherapy within 90 days of colectomy (12,13). Distance is based on 1-way travel.

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important to involve PCPs in the long-term care of cancer 8 0 10 66 84 na na na ND survivors (18). Availability of 24-hour helpline at childhood cancer centres is necessary to support PCPs and give caregivers direct communication with oncologists at

0 0 0 0 0 any time. Travel and accommodation support should be 20 20 20

border integrated into the cancer care of children in Saudi Arabia. Northern Our study was limited by the lack of data on the date of first appearance of symptoms and signs of cancer 6 0 0 0 0 17 23 23 compared to dates of diagnosis and starting treatment Albaha in order to measure accurately the impact of travel burden on the time to initiate cancer treatment. There 3 0 0 0 0 25 28 28 are inconsistent reports on the association between time Najran to diagnosis or treatment and poor survival in childhood cancer (19,20). Another study limitation was enrolling 8 0 0 0 0 31 39 39 only patients who were treated at cancer centres. Thus, Tabuk we could not assess potential early mortality among children with cancer living in rural areas prior to their 1 3 0 0 0 44 44 40 acceptance in cancer centres. Early death within the first Aljouf month of diagnosis in childhood cancer was associated with age < 1 year, low socioeconomic status, and certain 2 0 0 0 13 57 57 42

Hail cancers such as acute myeloid leukaemia (21). 6 6 0 0 16 41 63 na Conclusion

Qassim The travel burden on children with cancer and their families in Saudi Arabia is substantial. Approximately two Regions (patient’s home) 0 0 0 0 18 67 67 49 thirds of patients live in cities different from where the Jazan cancer centres are located. One third of patients are > 3 hours away (≥ 400 km) from cancer centres. Our findings 0 0 0 0 13 89 102 102

Asir might guide policy-makers to develop national strategies to improve access to childhood cancer care in Saudi Ara- bia. Future studies are needed to assess the impact of liv- 1 0 0 0 71 36 ing remotely from cancer centres on different outcomes 108 108 such as event-free and overall survival. Madinah Funding: The study was funded by Sanad Children’s Cancer Support Association Research Grant Programme. 1 3 23 78 70 82 na 175

Eastern Competing interests: None declared. 1 0 31 32 na 155 149 336 Figure 2 Regional referral pattern of childhood cancer in

Makkah Saudi Arabia. Childhood cancer centres are present in 4 circled cities. Arrows represent common referral patterns from each region. The weight of the arrow corresponds to the 3 5 2 0 73 na 511 433 proportion of patients referred to a specific region. Riyadh Regional referral pattern in childhood cancer Saudi Arabia Riyadh Makkah Eastern Qassim Features No. of patients Treatment centre – same city Treatment centre – same region but different city Treatment centre – different region Table 3

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Poids des déplacements et accès géographique aux soins de santé pour les enfants atteints de cancer en Arabie saoudite Résumé Contexte : Le poids des déplacements a un impact psychosocial et financier considérable sur les enfants atteints de cancer et sur leurs familles. Objectifs : La présente étude avait pour objectif d’étudier la répartition géographique du cancer chez l’enfant et d’évaluer le poids des déplacements pour les soins en Arabie saoudite. Méthodes : Il s’agissait d’une étude transversale multi-institutionnelle portant sur 1657 enfants atteints de cancer, diagnostiqués entre 2011 et 2014. Le type/stade du cancer, la ville/région de résidence et la ville/région du centre de traitement ont été enregistrés. Le poids des déplacements a été mesuré sur la base de la distance en kilomètres, dans un sens, entre le centre de la localité et l’établissement de soins. Cette étude a reçu le soutien de Sanad Children’s Cancer Support Association. Résultats : Les diagnostics concernaient la leucémie (45,2 %), les tumeurs solides hors système nerveux central (30,2 %), le lymphome (12,3 %), les tumeurs du système nerveux central (11,8 %) et l’histiocytose (0,5 %). Les centres de lutte contre le cancer de l’enfant se trouvaient dans la même ville que celle où les patients vivaient dans 652 cas (39,3 %), dans la même région, mais dans des villes différentes dans 308 cas (18,6 %) et dans des régions différentes dans 613 cas (37 %). Ce lieu n’était pas connu dans 84 cas (5,1 %). La distance moyenne parcourue par trajet pour les patients qui vivaient dans des régions différentes était de 790 km (distance comprise entre 116 et 1542 km). Au total, 536 patients (32 %) vivaient à 400 km du centre de traitement et 216 (13 %) à plus de 1000 km. Parmi les 642 patients atteints de leucémie lymphoblastique aiguë ayant nécessité deux à trois ans de traitement, 197 (31 %) vivaient à une distance supérieure ou égale à 400 km du centre de traitement et 94 (15 %) à plus de 1000 km. Conclusions : Près des deux tiers des patients atteints d’un cancer de l’enfant vivaient dans des villes différentes des centres de traitement, dont un tiers des patients à une distance supérieure ou égale à 400 km. Il est nécessaire d’élaborer des stratégies visant à améliorer l’accès aux soins des enfants atteints de cancer.

عبء السفر وإتاحة الرعاية الصحية باملناطق اجلغرافية التي يعيش فيها األطفال املصابون بالرسطان يف اململكة العربية السعودية عبد الرمحن السلطان، عبد اهلل اجلفري، مهاب إياس، موسى احلريب، نواف اخلياط، فيصل العنزي، فواز ياسني، فواز القاسم، قاسم احلريب، شاكر عبد اهلل، حممد أبرار، واصل جستنيه اخلالصة اخللفية: يؤثر عبء السفر ًتأثريا ًنفسيا ًواجتامعيا ًكبريا، ويفرض ً ضغوطامالية عىل مرىض رسطان األطفال ُوأرسهم. األهداف: هدفت هذه الدراسة إىل دراسة التوزيع اجلغرايف لرسطان األطفال وتقييم عبء السفر الذي تستلزمه الرعاية يف اململكة العربية السعودية. طرق البحث:أجريت هذه الدراسة املقطعية يف مؤسسات متعددة كام َّضمت 1657 ًطفال ًمصابا بالرسطان، ُش ِّخصت إصاباهتم باملرض بني َعام ْي 2011 و2014. ُوس ِّ ل نوع/ج مرحلة الرسطان ومدينة/ منطقة اإلقامة واملدينة/ املنطقة التي يقع فيها مركز العالج. وتم قياس عبء السفر عىل أساس مسافة أحادية االجتاه َّ رة مقدبالكيلومرتات من وسط املدينة إىل مؤسسة ِّتلقي العالج. َّوتلقت الدراسة َ منالدعم مجعية سند اخلريية لدعم األطفال املرىض بالرسطان. النتائج: شمل التشخيص رسطان الدم )45.2٪(، واألورام الصلبة التي تصيب ًأجهزة أخرى غري اجلهاز العصبي املركزي )30.2٪(، واللمفوما )12.3٪(، وأورام اجلهاز العصبي املركزي ) ٪( 11.8وكثرة اخلاليا املنسجة ) ٪(. 0.5وكانت مراكز رسطان األطفال تقع يف املدينة نفسها التي يعيش فيها املرىض يف 652 حالة ) ٪(، 39.3وتقع يف املنطقة نفسها ولكن يف مدينة خمتلفة يف 308حاالت ) ٪(،18.6 وتقع يف مناطق خمتلفة يف 613 حالة )37٪(، ومل يكن مكان مركز رسطان األطفال ً معروفايف 84 حالة ) ٪(.5.1 وكان متوسط مسافة السفر أحادية االجتاه للمرىض الذين ≥ يعيشون يف مناطق خمتلفة 790)املدى، (1542-116 ً.كيلومرتا ويعيش ما جمموعه 536 ًمريضا )32%( عىل ُبعد 400كم من مركز العالج، ويعيش 216 ًمريضا )13%( عىل ُبعد مسافة تزيد عن 1000 كم من مركز العالج. ومن بني 642 ًمريضا مصابني برسطان الدم الليمفاوي احلاد ≥ والذين حيتاجون إىل مدة عالج ترتاوح بني َعام ْ نيإىل ثالثة أعوام، كان 197 )31%( منهم يعيشون عىل ُبعد 400 كم من مركز العالج، ويعيش 94 )15%( منهم عىل ُبعد مسافة تزيد عن 1000كم من مركز العالج. االستنتاجات: يعيشما يقرب من ثلثي املرىض املصابني برسطان األطفال يف غري املدينة التي يقع فيها مركز العالج، ومن بني هؤالء يعيش ثلث ≥ املرىض عىل ُبعد 400 كيلومرت من مركز العالج. لذا َث َّمةحاجة إىل وضع اسرتاتيجيات لتحسني إتاحة الرعاية لألطفال املصابني بالرسطان.

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1361 Research article EMHJ – Vol. 26 No. 11 – 2020

Prevalence of refractive error and visual impairment among school-age children of Hargesia, Somaliland, Somalia

Zahra Abdi Ahmed,1 Saif Hassan Alrasheed2,3 and Waleed Alghamdi3

1Department of Primary Eye Care, Faculty of Optometry and Visual Sciences, Al-Neelain University, Khartoum, Sudan. 2Department of Binocular Vision, Faculty of Optometry and Visual Sciences, Al-Neelain University, Khartoum, Sudan (Correspondence to: Saif Alrasheed: [email protected]). 3Department of Optometry, College of Applied Medical Sciences, Qassim University, Qassim, Saudi Arabia.

Abstract Background: Childhood visual impairment is a global public health problem, especially in low and middle-income countries. Its most common causes are avoidable by early diagnosis and treatment. Aims: To assess prevalence of refractive error and visual impairment among school-aged children in Hargeisa, Somali- land, Somalia. Methods: This was a cross-sectional study of 1204 students (aged 6–15 years) in 8 randomly selected primary schools in Hargeisa from November 2017 to January 2018. We used the modified Refractive Error Study in Children to determine prevalence of refractive error and visual impairment, including the following investigations: distance visual acuity, assessed by Snellen Tumbling E-chart; refraction, assessed by retinoscope binocular vision assessment; and examination of anterior and posterior segments. Results: Prevalence of uncorrected, presenting and best-corrected visual impairment of 6/12 or worse was 13.6%, 7.6% and 0.75%, respectively. Only 16 of 91 (17.6%) children were using spectacles and the rest were unaware of the problem. Refrac- tive error was the cause of visual impairment in 76.8% of participants, amblyopia in 22.0%, trachoma in 2.4%, and corneal opacity and cataract in 0.6%. Anterior segment abnormalities were found in 8.3%, mainly vernal keratoconjunctivitis, while posterior abnormalities were observed in 0.7%. Prevalence of myopia was 9.1%, hypermetropia 2.7% and astigmatism 3.9%. Prevalence of visual impairment because of Refractive Error was associated with increasing age, but there was no significant association with school grade or sex. Conclusion: Prevalence of visual impairment among school-aged children in Hargeisa was high, and the leading cause was uncorrected Refractive Error. There are barriers to care and it is critical that they are overcome. Keywords: refractive error, childhood visual impairment, myopia, hypermetropia, vernal keratoconjunctivitis Citation: Abdi Ahmed Z; Alrasheed SH; Alghamdi W. Prevalence of refractive error and visual impairment among school-age children of Hargesia, Somaliland, Somalia. East Mediterr Health J. 2020;26(11):1362-1370. https://doi.org/10.26719/emhj.20.077 Received: 18/03/19; 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 defines VI in children as presenting with visual acuity (VA) less than 6/12 in the better eye. However, uncor- Globally, it is estimated that there are 36 million people rected VA (UVA) is defined as VA less than 6/12 in one or who are blind, 216.6 million have moderate to severe both eyes (7). VI among children in developing countries visual impairment (VI) and 188.5 million have mild VI. is a priority of eye health programmes, including Vision The leading cause of VI is uncorrected refractive error 2020: the Right to Sight Initiative (9). Globally, the prin- (RE) (1,2). Furthermore, 90% of people with VI live in de- cipal cause of VI is uncorrected REs (43%) and cataracts veloping countries. Almost 19 million children aged < 15 (33%) (1). Special attention should be given to children, years have VI globally. In developing countries, 7–31% of because VI restricts their education and general perfor- childhood blindness is avoidable, 10–58% is treatable, and mance, personality development, future quality of life 3–28% is preventable (3). RE is an eye condition in which light from a distant object is not focused on the retina; it and career opportunities (10). The Refractive Error Study might be focused in front of or behind the retina. There in Children (RESC) protocol was developed by WHO in are 3 types of RE: myopia, hypermetropia and astigma- collaboration with, and under financial support from the tism. The exact cause of ametropia remains unknown National Eye Institute, National Institutes of Health and with common risk factors being hereditary, nutritional the United States of America to assess the prevalence of and environmental (4). Population-based studies on VI VI and RE worldwide, as well as to assess the effect of and RE in children have been conducted on populations childhood VI due to uncorrected RE (11,12). with different racial backgrounds and environments in Somaliland, Somalia has a population of 4.5 million, Africa. These studies have shown that the prevalence of with estimated urban poverty of 29%, which is similar VI among children was 2.15% in South Africa (5), 5.5% in to 26% in Ethiopia. Only about half of children aged Khartoum, Sudan (6), 4.4% in South Darfur, Sudan (7), and 6–13 years go to primary school in Somaliland, in stark 9.5% in Ethiopia (8). World Health Organization (WHO) contrast to 87% in neighbouring Ethiopia (13,14). No

1362 Research article EMHJ – Vol. 26 No. 11 – 2020 studies have assessed VI and RE among school-aged Clinical investigation children in Hargeisa, Somaliland. The aims of this study The clinical examinations were performed using the were to assess the common causes of VI, types of RE, and modified RESC protocol. Demographic information differences in prevalence according to sex, age and school was collected from participants, and VA at distance was grade. measured using the Snellen Tumbling E-chart with E’s of standard size at a 6-m distance. Participants with VA ≤ Methods 6/12 were assessed by pinhole test, and if their vision improved, they underwent retinoscopy without cycloplegia Study design and subjective refraction. All children were examined by This was a cross-sectional, school-based study of VI and a penlight and low-power hand magnifier to assess any RE among children from Hargeisa, Somaliland. Accord- anterior-segment abnormalities in the eyelids, conjunc- ing to the Ministry of Education, the overall number of tiva, cornea, pupils and pupillary reflex reaction. A cover test was conducted for heterophoria or heterotropia and students enrolled in public and private primary schools the angle of deviation was measured using the corneal in Hargeisa during 2017–2018 was 243 485, comprising light reflex (Hirschberg test) and the Prism Cover Test at 127 829 boys and 115 656 girls. The modified RESC pro- distance and near fixation, respectively. The ocular mo- tocol was used to assess the prevalence of VI and RE in tility test was performed to assess eye muscle function. these children. Noncycloplegic refraction was used to as- Subjective refraction was determined using a standard sess the prevalence of RE, which is defined as follows: (1) refraction trial set to achieve best correct vision for chil- myopia ≥ −0.5 D in one or both eyes; (2) hypermetropia ≥ dren whose vision improved with the pinhole test. Chil- 2.0 D ; and (3) astigmatism ≥ 0.75 D cylindrical refraction dren with VA ≤ 6/12 whose vision did not improve by (11). pinhole test had outer eye and fundus examination by Inclusion and exclusion criteria direct ophthalmoscopy, and any abnormal findings were recorded as causes of VI. Children aged 6–15 years who attended school on the days of examination and their parents agreed to partic- Data analysis ipate in the study. Children unable to provide parental Data for each participant were analysed descriptively consent were excluded. using standard deviations and percentages with SPSS version 22. The relationship between measures was de- Study sample termined using correlation, cross-tabulations and χ2 anal- The study sample was selected through stratified multi- ysis. For all statistical determinations, significance levels stage sampling. We assumed a prevalence of RE of 5% were established at P = 0.05. according to the estimated prevalence of childhood RE in Africa (5%), Sudan (6.8%) (5) and Kenya (5.1%) (15, 16). Results Considering a prevalance of RE of 5%, 95% confidence interval and maximum acceptable random sampling error Study population of 1.5%, a sample size of 811, based on the formula below, A total of 1351 children were selected to participate in the was estimated. Considering the design effect = 1.5, a final study and 1204 (89%) were actually entered into the study. sample of 1216 was estimated. Demographic characteristics of participants 2 2 2 2 n = (z pq)/d = (1.96 × 0.05 × 0.95)/0.015 = 811 => 811 × 1.5 = 1216 The 1204 participants were aged 6–15 years, with a mean Considering a nonresponse rate = 10%, the final sample of 11.18 [standard deviation (SD); 2.45] years (Table 1). There were 658 (54.7%) boys and 546 girls (45.3%). The size was 1351 schoolchildren. The study sample com- mean (SD) age of the boys and girls was 11.15 (2.47) and prised 8 schools (4 for boys and 4 for girls) that were ran- 11.21 (2.44) years, respectively. Most participants were domly selected from 22 districts of Hargesia. One class aged 11 (14.2%) and 12 (13.7%) years, respectively. The ages from each grade (1–8) with a minimum of 21 children was with the fewest participants were 6 (3.2%) and 7 (5.1%) randomly chosen. years, respectively. There was no significant difference Ethical considerations in mean age between the boys and girls (ANOVA: F = 0.167, P = 0.683), although there was a significant differ- Ethical permission for the study was obtained from Al- ence in mean ages of the children according to school Neelain University, Khartoum, Sudan because of un- grades (ANOVA: F = 341.733, P = 0.01). availability of an ethics committee in Somaliland. The study was conducted according to the Declaration of Hel- Distribution of ocular signs and symptoms sinki guidelines. Informed consent was obtained from all A total of 943 (78.8%) participants did not complain of participants. All forms and data sheets were shredded as any ocular symptoms; 153 (12.7%) complained of blurred soon as the details were entered into the database system vision; 87 (7.2%) had itching and redness; and 15 (1.2%) had for analysis. pain and photophobia.

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Table 1 Demographic characteristic of participants Age (years) Sex Total Male Female n % n % n % 6 20 3.0 18 3.3 38 3.2 7 35 5.3 27 4.9 62 5.1 8 58 8.8 40 7.3 98 8.1 9 58 8.8 57 10.4 115 9.6 10 95 14.4 62 11.4 157 13.0 11 92 14.0 79 14.5 171 14.2 12 80 12.2 85 15.6 165 13.7 13 83 12.6 66 12.1 149 12.4 14 71 10.8 58 10.6 129 10.7 15 66 10.1 54 9.9 120 10.0 Total 658 546 1204

VA alence of VI (2%, 95% CI, 1.2–2.8%) than those aged 10–11 years (3.4%, 95% CI, 2.4–4.4%), and the highest prevalence A total of 1044 children presented with normal vision (6/6) in the right eye; 1034 had normal vision in the was in children aged 14–15 years (4.4%, 95% CI, 3.2–5.7%). left eye; and 1071 had normal vision in the better eye Binocular anomalies (Table 2). Thirty-six, 38 and 42 children had uncorrected vision (6/9) in the right, left and better eye, respective- Tropia was found in 9 (0.7%) children: 4 with esotropia ly. An uncorrected VI was found in 164 children (13.6%, and 5 with exotropia. 95% CI, 11.7–15.5%), while 91 (7.6%, 95% CI, 6.1–9.1%) chil- Anterior-segment examination dren had VI. With best-corrected VA, this decreased to 9 (0.75%, 95% CI, 0.3–1.2%) children. A total of 1104 children (91.7%, 95% CI, 90.1–93.3%) had no abnormalities detected in the right eye and 1103 (91.6%, Prevalence of VI 95% CI, 90.0–93.2) had no abnormalities in the left eye. The prevalence of presenting VI was 91 (7.6%, 95% CI, Ninety-seven children (8.1%, 95% CI, 6.6–9.6%) had vernal 6.1–9.1%) and only 16 (17.6%) of these children were wear- keratoconjunctivitis in both eyes. Three children (0.25%, ing spectacles. There were no significant association be- 95% CI, 0.03–0.5%) had trachoma in the left eye and 2 tween prevalence of VI and age (P = 0.209), sex (P = 0.060) (0.2%, 95% CI, 0.1–0.5%) had trachoma in the right eye. and school grade (P = 0.393). Girls had a higher prevalence One child had cataract in the right eye (0.1%, 95% CI, −0.1 of VI (4.6%, 95% CI, 3.4–5.8) than boys had (2.6%, 95% CI, to 0.3%) and one (0.1%, 95% CI, 0–0.3%) had corneal opaci- 1.7–3.5%). Younger children age 6–7 years had lower prev- ty in the left eye.

Table 2 Distribution of uncorrected visual acuity for right, left and better eye by percentage and confidence interval UVA Right eye Left eye Better eye Best-corrected VA

n % (95% CI) n % (95% CI) n % (95% CI) n % (95% CI) 6/6 1044 86.7 (84.8–88.6) 1034 85.9 (83.9–87.9) 1071 89.0 (87.2–90.8) 1182 98.1 (97.5–99.0) 6/9 36 3.0 (2.0–4.0) 38 3.2 (2.2–4.2) 42 3.5 (2.5–4.5) 13 1.08 (0.5–1.7) 6/12 21 1.7 (1.0–2.4) 28 2.3 (1.5–3.2%) 24 2.0 (1.2–2.8) 3 0.25 (0.03–0.53) 6/18 32 2.7 (1.8–3.6) 32 2.7 (1.8–3.6) 31 2.6 (1.7–3.5) 2 0.17 (0.0–0.4) 6/24 29 2.4 (1.5–3.3) 32 2.7 (1.8–3.6%) 19 1.6 (0.9–2.3) 2 0.17 (0.0–0.4) 6/36 23 1.9 (1.13–2.67) 19 1.6 (0.9–2.3) 9 0.7 (0.2–1.2) 2 0.17(0.0–0.4) 6/60 12 1.0 (0.4–1.6) 13 1.1 (0.5–1.7) 4 0.3 (0.01–0.61) — — CF 6 0.5 (0.1–0.9) 7 0.6 (0.16–1.04) 4 0.3 (0.01–0.61) — — HM 1 0.1 (0.0–0.3) 1 0.1 (0.0–0.3) — — — —

Total 1204 100.0% 1204 100% 1204 100.0% 1204 %100.0 VA ≥ 6/12 91 7.6 (6.1–9.1) 9 0.75(0.3–1.2) CF = count fingers; CI = confidence interval; HM = hand movement; UVA = uncorrected visual acuity; VA = visual acuity.

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Prevalence of RE Posterior-segment examination A total of 189 children (15.7%, 95% CI, 13.7–17.8%) had Posterior-segment examination revealed that 1196 chil- REs, and 1015 (84.3%, 95% CI, 82.3–86.4%) were emme- dren (99.3%, 95% CI, 98.8–99.8%) had no abnormalities. tropic (Table 3). Myopia had the highest prevalence Ocular media and fundus abnormalities were seen in 8 (0.7%) children. Retinal disorders were found in 6 (0.5%) (n = 110, 9.1%), followed by astigmatism (n = 47, 3.9%) and children and media opacity in 2 (0.2%). hypermetropia (n = 32, 2.7%). The prevalence of RE was significantly associated with age (P = 0.011) but not sex Principal causes of VI (P = 0.073) or school grade (P = 0.168). Prevalence of REs was The causes of UVA of 6/12 or worse at least in 1 eye are higher among girls (n = 100, 18.3%) than boys (n = 89, 13.5). presented in Table 4. RE was the main cause of VI in 126 Prevalence of REs significantly increased with age. Chil- (76.8%) affected children, followed by amblyopia (n = 36, dren aged 15 years had the highest prevalence (n = 21; 22.0%) and corneal opacity and cataract (n = 1, 0.6%). 17.5%), compared to those aged 8 years (n = 14, 14.3%), Schoolchildren who received eye drops or were 7 years (n = 10, 16.1%) and 6 years (n = 5, 13.2%). Children referred in school grade 4 had the highest prevalence of REs (n = One hundred and forty-two children (11.8%, 95% CI, 10.0– 33, 21.9%), and those in grade 2 had the lowest prevalence 13.6%) had uncorrected REs and were referred to Manhal (n = 16, 10.7%). The prevalence of myopia was increase Specialist Hospital, Hargeisa. Two children were referred with age; it was more common in children aged 15 years for further examination and treatment of media opacity. (10.8%) than in those aged 6 (5.3%), 7 (8.1%) and 8 (7.1%) Eighty-seven children (7.2%, 95% CI, 5.7–8.7%) were pre- years. In contrast, prevalence of hypermetropia was scribed eye drops, and 15 (1.2%, 95% CI, 0.6–1.8%) received highest in children aged 6 years (5.3%), and lowest in only advice for their complaints. those aged 15 years (0.8%). According to the gender the prevalence of myopia, hypermetropia and astigmatism Discussion was higher in girls at 10.3, 2.7 and 5.3%, respectively, than Childhood blindness and VI are priority conditions tar- in boys at 8.2, 2.6 and 2.7%, respectively. geted in Vision 2020: the Right to Sight Initiative of WHO

Table 3 Prevalence of refractive error in one or both eyes by age, sex and school grade Category Emmetropia Myopia Hypermetropia Astigmatism no funds reflex Total (95% CI, 82.3–86.4) (95% CI, 7.5–10.7) (95% CI, 1.8–3.6) (95% CI, 2.8–5.0) (95% CI, 1.4–1.6) n % n % n % n % n % n % Age 6 33 86.8 2 5.3 2 5.3 1 2.6 0 0 38 3.2 ( P = 0.011) 7 52 83.9 5 8.1 3 4.8 2 3.2 0 0 62 5.1 8 84 85.7 7 7.1 5 5.1 2 2.0 0 0 98 8.1 9 100 87.0 9 7.8 5 4.3 1 0.9 0 0 115 9.6 10 132 84.1 14 8.9 4 2.5 7 4.5 0 0 157 13.0 11 145 84.8 17 9.9 2 1.2 7 4.1 0 0 171 14.2 12 136 82.4 17 10.3 6 3.6 6 3,6 1 0.6 165 13.7 13 129 86.6 13 8.7 2 1.3 5 3.4 0 0 149 12.4 14 105 81.4 13 10.1 2 1.6 9 7.0 0 0 129 10.7 15 99 82.5 13 10.8 1 0.8 7 5.8 0 0 120 10.0 Sex M 569 90.6 54 8.2 17 2.6 18 2.7 0 0 658 54.7 ( P = 0.073) F 445 81.5 56 10.3 15 2.7 29 5.3 1 0.2 546 45.3 Class level 1 129 87.2 6 4.1 7 4.7 6 4.1 0 0 148 12.3 ( P = 0.168) 2 134 89.3 10 6.7 3 2.0 3 2.0 0 0 150 12.5 3 122 81.3 17 11.3 7 4.7 4 2.7 0 0 150 12.5 4 118 78.1 22 14.6 3 2.0 7 4.6 1 0.7 151 12.5 5 130 86.1 12 8.0 4 2.6 5 3.3 0 0 151 12.5 6 130 85.5 11 7.2 3 2.0 8 5.3 0 0 152 12.6 7 122 80.8 18 11.9 3 2.0 8 5.3 0 0 151 12.5 8 129 85.4 14 9.3 2 1.3 6 4.0 0 0 151 12.5 Total 1015 84.3 110 9.1 32 2.7 47 3.9 1 0.1 1204 100% CI = confidence interval.

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Table 4 Causes of uncorrected visual acuity 6/12 or worse Causes Children with VA 6/12 or worse in one Prevalence in the population in one or both eyes, or both eyes % (95% CI) n % Refractive error 126 76.8 10.5 (8.8–12.2) Amblyopia 36 22.0 3.0 (2.04–4.0) Corneal opacity 1 0.6 0.08 (−0.08 to 0.24) Cataract 1 0.6 0.08 (0.08–0.24) Any cause 164 100.0 13.6 (11.7–15.5) CI = confidence interval; VA = visual acuity.

(17). Knowledge of the prevalence of RE and VI among The prevalence of myopia was 9.1%, which is higher school age children can help the relevant authorities to than 6.0% in Ethiopia (24) but lower than 14.1% in Ghana plan and provide eye care services in the particular geo- (30). In our study, older school children had a higher graphical area. The present study attempted to provide prevalence of myopia, which was similar to a study in this information, as well as being the first study in So- Viet Nam (32). Alrasheed et al. (7) attributed this age- maliland to assess the prevalence of the VI and RE among associated increase in myopia with decreased outdoor school-aged children. activity of many children and this has been reported as Noncycloplegic refraction was used to assess REs an issue in other studies (5,25,32). in this study, similar to studies of school-aged children The prevalence of hypermetropia in this study was in Nigeria (18) and South Africa (19). Noncycloplegic 2.7%, which is significantly lower than that reported refraction was chosen so as not to interfere with the in studies in Ethiopia 26.4% (24) and Saudi Arabia 6.9% academic activity of the children. (35). However, it is higher than in South Africa (1.8%) (10) The prevalence of VI in the present study was 7.6%, and China (1.6%) (36) but similar to Tunisia (2.61%) (37). which is lower than 10.1% in Malaysia (20) and 10.3% in The lower prevalence of hypermetropia in our study China (21), but higher compared with 1.2% in South Africa might have been due to use of noncycloplegic refraction, (5) 1.2%, 2.67% in South America (22) and 3.5% in the Islamic which could have missed a significant number of cases Republic of Iran (23). These results indicate that VI among of hypermetropia. The prevalence of hypermetropia school-aged children requires urgent intervention by the decreased with age and was higher in children aged 6 and community and nongovernmental organizations. The 7 years compared with 14 and 15 years. This result agreed results also reflect lack of childhood eye care services in with Chebil et al. (37), who reported that this variation this region as well as lack of community awareness about could be related to a decrease in the dioptric power of the the consequences of childhood VI. lens (it goes form 23 D at age 3 years to 20 D at 14 years), or with an increase in the optical density of the crystalline In the present study, the prevalence of VI was higher cortex. among girls than boys (4.6% vs 2.6%), which agrees with a study in Ethiopia (3.2% for girls and 2.6% for boys) (24). The prevalence of astigmatism in the current study This might have been due to socioeconomic factors that was 3.9%. This is lower than that found in the Islamic contributed to better access to health services for boys. Republic of Iran (6.6%) (38) and South Africa (14.6%) (5) but However, the difference was not significant. similar to that in Poland (4%) (39). The prevalence of RE in either eye was 15.7%, which The prevalence of manifest strabismus was 0.7%, is lower than that in Ghana (25.6%) (25), India (25.1%) which is similar to that among children in the United

(26), Egypt (22.1%) (27) and Qatar (19.7%) (28), but higher Republic of Tanzania (0.5%) (40) butlower than in Iranian than in Uganda (11.6%) (29), Ghana (13.3%) (30) and Saudi school children (1.2%) (41). Arabia (13.7%) (31). The prevalence of RE in our study was In this study, uncorrected RE was the most common similar to that in Viet Nam (16.3%) (32) and Saudi Arabia cause of VI among children, and was responsible for (16.3%) (33). This variation may be related to the type of 76.8% of cases. This is similar to other studies that used sampling method used, size of population screened, and RESC protocol, such as in Ethiopia (77.3%) (24) and India variation in geographic location. We found no significant (77%) (26) but lower than in Malaysia (87.0%) (20) and in association between prevalence of RE and school grade the Islamic Republic of Iran (87.3%) (23). Alrasheed et al. (7) or sex. However, we did show that the prevalence of VI suggested that this could have been because of genetic caused by uncorrected RE increased significantly with differences as well as different lifestyles in terms of age. Nevertheless, we found that prevalence of RE was outdoor activities. The second most frequent cause of VI higher among girls than boys (81.3% vs 13.5%), which, as among children was amblyopia at 22.0%, which is higher mentioned above, might have been due to better access than in Sudan (5.6%) (6) and South Africa (9.6%) (4). This to health care for boys in this culture. This is consistent may be due to the high rate of poverty and illiteracy in with a similar study in Saudi Arabia (34). Somaliland and the poor health system in the country.

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In the present study, out of 91 children with VI, only and seventh grades, and children aged 6 and 7 years were 16 (17.6%) were already using spectacles, while the rest less prevalent in this study, because many children in were not aware of the problem. This may have been due Somaliland start school later than the recommended to lack of child and parental awareness of the vision 6 years. Fifth, Log Mar charts were not available, so problem, attitudes regarding the need for spectacles, cost we used Snellen Tumbling E-charts, and slit lamps of spectacles, cosmetic appearance, peer pressure and and fundus biomicroscopy were not easy to transport concerns that wearing glasses may cause progression of RE (42,43). between locations, so they were replaced by torch and magnifier, and ophthalmoscopy. Finally, RE was assessed This study had several limitations. First, a large by noncycloplegic refraction, which could have missed a number of schools were not registered with the Ministry of Education in Hargeisa, so the study sample did not significant number of cases of hypermetropia. include all schools. Second, almost half of school-age children were not attending school due to poverty, thus Conclusions the study only included children who attended school. Third, places of study and examination differed among The prevalence of VI among school-aged children in Har- schools in terms of lighting, ventilation and comfort. geisa, Somaliland was high and the commonest causes Fourth, distribution of children’s ages at school levels was were uncorrected REs. There are barriers to care and it is not uniform, so older children were not only in the eighth critical that they are overcome.

Acknowledgement We are grateful to all schools included in this study and their staff for help with data collection. We also thank all the students who participated in this study and their parents, as well as the students of the Faculty of Optometry and Visual Science, University Of Hargeisa. We are grateful to Manhal Specialist Hospital ,which provided us with the required in- strumentation, and free treatment for any student who was referred to the hospital. Funding: None. Competing interests: None declared.

Prévalence du vice de réfraction et de la déficience visuelle chez les enfants d’âge scolaire de Hargesia, au Somaliland (Somalie) Résumé Contexte : Les troubles visuels chez l’enfant constituent un problème de santé publique mondial, en particulier dans les pays en développement. Ses causes les plus courantes sont évitables par un diagnostic précoce et la mise en place rapide d’un traitement. Objectifs : La présente étude avait pour objectif d’évaluer la prévalence du vice de réfraction et de la déficience visuelle chez les enfants d’âge scolaire à Hargeisa, au Somaliland (Somalie). Méthodes : Il s’agissait d’une étude transversale menée auprès de 1204 élèves (âgés de 6 à 15 ans) de huit écoles primaires sélectionnées de manière aléatoire à Hargeisa, entre novembre 2017 et janvier 2018. Nous avons utilisé l’étude modifiée sur le vice de réfraction chez les enfants afin de déterminer la prévalence de cette affection et de la déficience visuelle, comprenant les examens suivants : acuité visuelle à distance, évaluée par l’échelle de Snellen avec des E ou C directionnels ; la réfraction, évaluée par examen de la vision binoculaire par rétinoscopie ; et examen des segments antérieurs et postérieurs. Résultats : La prévalence de la déficience visuelle non corrigée, détectée et la mieux corrigée de 6/12 ou un score inférieur était respectivement de 13,6 %, de 7,6 % et de 0,75 %. Seuls 16 enfants sur 91 (17,6 %) portaient des lunettes tandis que les autres n’avaient pas conscience du problème. Le vice de réfraction était la cause de la déficience visuelle chez 76,8 % des participants, l’amblyopie dans 22,0 % des cas, le trachome chez 2,4 % des enfants, et l’opacité cornéenne et la cataracte chez 0,6 % d’entre eux. Des anomalies du segment antérieur ont été observées chez 8,3 % des participants à l’étude, principalement des kératoconjonctivites vernales, tandis que des anomalies du segment postérieur ont été observées dans 0,7 % des cas. La prévalence de la myopie était de 9,1 %, celle de l’hypermétropie de 2,7 % et celle de l’astigmatisme de 3,9 %. La prévalence de la déficience visuelle due à un vice de réfraction était associée à un âge supérieur, sans toutefois que l’on puisse noter de corrélation significative avec le niveau scolaire ou le sexe. Conclusion : La prévalence de la déficience visuelle chez les enfants d’âge scolaire de Hargesia était élevée, principalement en raison d’un vice de réfraction non corrigé. Il existe des obstacles aux soins et il est essentiel de les surmonter.

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معدل انتشار اخلطأ االنكساري وضعف البرص بني األطفال يف سن الدراسة يف هرجيسا، صوماليالند )الصومال( زهرة عبدي أمحد، سيف الرشيد، وليد الغامدي اخلالصة اخللفية: ُي َع ُّ دضعف البرص يف مرحلة الطفولة ًمن مشكلةمشكالت الصحة العامة عىل الصعيد العاملي، وال َّام سييف البلدان املنخفضة الدخل. ويمكن جتنب أسبابه األكثر ًشيوعا عن طريق التشخيص والعالج ُامل َبكر ْين. األهداف: هدفت هذه الدراسة إىل تقييم معدل انتشار اخلطأ االنكساري وضعف البرص بني األطفال يف سن الدراسة يف هرجيسا، صوماليالند )الصومال( طرق البحث: شملت هذه الدراسة املقطعية 1204طالب )ترتاوح أعامرهم بني 6 سنوات و15 سنة( يف 8 مدارس ابتدائية خمتارة ً عشوائيايف هرجيسا خالل الفرتة من نوفمرب/ ترشين الثاين 2017 إىل يناير/كانون الثاين . 2018واستخدمنا دراسة اخلطأ االنكساري َّاملعدلة لدى األطفال

لتحديد معدل انتشار اخلطأ االنكساري وضعف البرص، بام يف ذلك االستقصاءات التالية: حدة البرص عن ُبعد، التي تم تقييمها بواسطة خمطط Snellen ، Tumbling E-chartواالنكسار، الذي تم تقييمه من خالل تقييم رؤية العينني بمنظار الشبكية، وفحص األجزاء األمامية واخللفية. النتائج: بلغ معدل انتشار ضعف البرص بقيمة 6/ 12أو أقل غري ُامل َّصحح ُوامل ِستعلن ُوامل َّصحح عىل أفضل وجه 13.6% و7.6% و %0.75 عىل التوايل. وكان 16 فقط من بني 91 ًطفال ) %( 17.6يستخدمون النظارات وكان الباقون غري مدركني للمشكلة. وكان سبب ضعف البرص هو اخلطأ االنكساري يف % 76.8من املشاركني، َوالغ َمش يف % 22.0منهم، والرتاكوما يف 2.4% منهم، َوع َتامة َالق ْرنِ َّية ّ والساديف % 0.6من املشاركني. ُووجدت تشوهات يف اجلزء األمامي يف 8.3٪من املشاركني، وعىل وجه اخلصوص التهاب َالق ْرنِ َّة يوامللتحمة الربيعي، يف حني لوحظت تشوهات يف اجلزء اخللفي يف 0.7٪ منهم. وبلغ معدل انتشار َاحل َس 9.1%، ومد البرص 2.7%، والالبؤرية 3.9%. وارتبط معدل انتشار ضعف البرص الناجم عن اخلطأ االنكساري بزيادة العمر، ولكن مل يكن هناك ارتباط مهم بالصف املدريس أو نوع اجلنس. االستنتاجات: كان معدل انتشار ضعف البرص بني األطفال يف سن الدراسة يف هرجيسا ًمرتفعا، وكان السبب الرئييس وراءه اخلطأ االنكساري غري ُامل َّصحح. َوث َّمة عوائق حتول دون تقديم الرعاية، ومن األمهية بمكان أن يتم التغلب عليها.

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Prevalence of refractive errors among pre-school children at King Abdulaziz Medical City, Riyadh, Saudi Arabia. Saudi Journal of Ophthalmology. 2010 Apr;24(2):45–8. http://dx.doi.org/10.1016/j.sjopt.2010.01.001 PMID:23960874 36. Li Z, Xu K, Wu S, Lv J, Jin D, Song Z, Wang Z, Liu P. Population‐based survey of refractive error among school‐aged children in rural northern China: the Heilongjiang Eye Study. Clin Exp Ophthalmol. 2014 May–Jun;42(4):379–84. http://dx.doi.org/10.1111/ ceo.12198 PMID:23952961 37. Chebil A, Jedidi L, Chaker N, Kort F, Limaiem R, Mghaieth F, et al. Characteristics of astigmatism in a population of Tuni- sian school-children. Middle East Afr J Ophthalmol. 2015 Jul–Sep;22(3):331–4. http://dx.doi.org/10.4103/0974-9233.150635 PMID:26180472

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38. Khalaj M, Gasemi M, Zeidi IM. Prevalence of refractive errors in primary school children [7–15 years] of Qazvin City. Eur J Sci Res. 2009;28(2):174–85. 39. Czepita D, Mojsa A, Ustianowska M, Czepita M, Lachowicz E. Prevalence of refractive errors in schoolchildren ranging from 6 to 18 years of age. Ann Acad Med Stetin. 2007;53(1):53–6. PMID:18561610 40. Wedner SH, Ross DA, Balira R, Kaji L, Foster A. Prevalence of eye diseases in primary school children in a rural area of Tanzania. Br J Ophthalmol. 2000 Nov;84(11):1291–7. http://dx.doi.org/10.1136/bjo.84.11.1291 PMID:11049957 41. Jamali P, Fotouhi A, Hashemi H, Younesian M, Jafari A. Refractive errors and amblyopia in children entering school: Shahrood, Iran. Optom Vis Sci. 2009 Apr;86(4):364–9. http://dx.doi.org/10.1097/OPX.0b013e3181993f42 PMID:19289975 42. Alrasheed SH, Naidoo KS, Clarke-Farr PC. Attitudes and perceptions of Sudanese high-school students and their parents towards spectacle wear. Afr Vis Eye Health. 2017 Apr 11;77(1):1–7. https://doi.org/10.4102/aveh.v77i1.392 43. Alrasheed SH, Naidoo KS, Clarke-Farr PC, Binnawi KH. Building consensus for the development of child eye care services in South Darfur State in Sudan using the Delphi technique. Afr J Prim Health Care Fam Med. 2018 Oct 24;10(1):1–9. http://dx.doi. org/10.4102/phcfm.v10i1.1767 PMID:30456975

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Risk factors associated with worse outcomes in COVID-19: a retrospective study in Saudi Arabia

Anas Khan,1,2 Saqer Althunayyan,3 Yousef Alsofayan,2 Raied Alotaibi,4 Abdullah Mubarak,4 Mohammed Arafat,1 Abdullah Assiri5 and Hani Jokhdar5

1Department of Emergency Medicine, College of Medicine, King Saud University, Riyadh, Saudi Arabia. 2Global Center for Mass Gatherings Medicine, Ministry of Health, Riyadh, Saudi Arabia. 3Department of Accident and Trauma, Prince Sultan Bin Abdulaziz College for Emergency Medical Services, King Saud University, Riyadh, Saudi Arabia. 4Department of Basic Science, Prince Sultan Bin Abdulaziz College for Emergency Medical Services, King Saud University, Riyadh, Saudi Arabia. 5Ministry of Health, Riyadh, Saudi Arabia. (Correspondence to: Yousef Alsofayan: [email protected]; [email protected]).

Abstract Background: The rapid emergence of the novel coronavirus disease 2019 (COVID-19) has resulted in millions of infected patients and hundreds of thousands of deaths worldwide. Health care services delivery is being compromised due to the surge in the number of infected patients during this pandemic. Aims: This study aimed to assess the risk factors associated with poor prognosis among COVID-19 patients in Saudi Arabia. Methods: This was a multi-centre retrospective cohort study that included all laboratory-confirmed COVID-19 cases with definitive outcomes in Saudi Arabia during March 2020. Demographic, clinical history, comorbidity and outcomes data were retrieved from the National Health Electronic Surveillance Network (HESN) database. We used logistic regression models to calculate crude and adjusted odds ratios (OR) to explore risk factors for critical outcomes (intensive care unit admission or death) among COVID-19 cases. Results: We included 648 COVID-19-positive patients with a median age of 34 years. Of these, 11.9% were in the critical group. Risk factors associated with worse outcomes included males (OR=1.92), age >60 years (OR=3.65), cardiac diseases (OR=3.05), chronic respiratory diseases (OR=2.29), and cases with two or more comorbidities (OR=2.57) after adjusting for age and sex; all had significant P-values <0.05. Conclusions: Independent risk factors for critical outcomes among COVID-19 cases include old age, males, cardiac patients, chronic respiratory diseases, and the presence of two or more comorbidities. We recommend designing a unique multi-item scale system to prognosticate COVID-19 patients. Keywords: COVID-19, risk factors, ICU admission, mortality, Saudi Arabia Citation: Khan A; Althunayyan S; Alsofayan Y; Alotaibi R; Mubarak A; Arafat M; et al. Risk factors associated with worse outcomes in COVID-19: a retrospective study in Saudi Arabia. East Mediterr Health J. 2020;26(11):1371–1380. https://doi.org/10.26719/emhj.20.130 Received: 24/06/20; accepted: 14/09/20 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 The clinical manifestation of COVID-19 is broad and ranges from asymptomatic and mild upper respiratory The rapid emergence of the novel Coronavirus Disease tract symptoms to severe illnesses with multiorgan 2019 (COVID-19) has resulted in millions of infected pa- failure and death (2–4). Furthermore, it is challenging tients and hundreds of thousands of deaths worldwide. to predict the clinical course or determine patients at In Saudi Arabia, the total number of confirmed COVID-19 risk of deterioration. Previous reports showed that old cases as of 13 June 2020 reached 123 308 confirmed cas- age and male gender are risk factors for disease severity es and 932 deaths and is increasing daily (1). Its spread and mortality (5,6). Other medical comorbidities are is becoming difficult to control and efforts should focus associated with poor prognoses such as cardiovascular on effective mitigation measures to minimize the disease disease, diabetes mellitus, chronic respiratory disease, impact on those prone to developing adverse outcomes. and hypertension (7,8). Moreover, distinct signs and Internationally, health-care services delivery is being symptoms or even laboratory findings are correlated with compromised due to the surge in the number of infected worse outcomes (5). Nevertheless, these studies’ results patients during this COVID-19 pandemic. Overwhelming are difficult to generalize in the Eastern Mediterranean the health-care system will lead to an unexpected rise in Region because the reported clinical predictors of morbidity and mortality of various treatable conditions. mortality were studied in different population groups, Therefore, it is critical to risk stratify COVID-19 patients and clinical characteristics can be different (9). based on their predicted outcomes and guide appropriate In this cohort study, we assessed the risk factors management and disposition accordingly. of ICU admission or death among COVID-19 patients

1371 Research article EMHJ – Vol. 26 No. 11 – 2020 in Saudi Arabia including clinical features, common test was significant using the Kolmogorov-Smirnov test comorbidities, and a number of laboratory findings. and the Shapiro-Wilk test. The non-parametric Mann Whitney U-test was used to compare two numerical Methods groups. Categorical variables underwent a test of association using the Chi-square test or Fisher exact test This retrospective cohort study collected data from all when the number of cases was small. laboratory-confirmed COVID-19 cases located in health Univariable and multivariable logistic regression care facilities across all regions of Saudi Arabia in March models were used to obtain the crude and the adjusted 2020. Health-care facilities are mandated to enter the odds ratio (OR) and their associated 95% confidence demographic, clinical, laboratory and outcomes data interval (CI). All percentages were rounded to one decimal of COVID-19-positive patients in the National Health place. The statistical significance was set to a P-value of < Electronic Surveillance Network (HESN) database by the health-care providers under the supervision of the 0.05. The analysis was done using Statistical Package for Ministry of Health (MoH). All confirmed cases of COV- the Social Sciences 24 (IBM-SPSS-24). ID-19 were screened and only patients with definitive outcomes were included; those in the active phase were Results excluded. Between 1–31 March 2020 a total of 1519 COVID-19-pos-� Demographic, clinical, laboratory, comorbidity, itive cases were screened, 648 patients with definitive and outcomes data of COVID-19 positive patients outcomes were included in the analysis; 11.9% (n=77) of were retrieved from the HESN database and extracted them were critical while 88.1% (n=571) were non-criti- into electronic sheets by two data collectors. Any cal (Figure 1). Out of the 77 critical patients, 15.6% (n=12) discrepancies were solved by a 3rd independent reviewer patients have died and 84.4% (n=65) have recovered based on the medical reports. In parallel with the World (Figure 1). The distribution of gender varied between Health Organization (WHO) protocols, COVID-19 was critical and non-critical groups where males constituted diagnosed based on the results of quantitative RT-PCR 67.5% (n=52) of the critical group versus 50.8% (n=290) testing from nasopharyngeal samples (10). We analyzed of the non-critical group, with a statistically signifi- age in three different forms: continuous, binary and 20- cant association P = 0.006. The median and IQR of age year intervals based on the risk stratification for severe differed significantly P = 0.001 across critical cases ver�- disease in patients with COVID-19 (11). Fever was defined sus non-critical cases with 37 years (27) and 33 years (18), as a temperature of 38 ֯C or higher, high respiratory rate respectively. Smoking was not associated with the worse was defined as more than 24 breaths per minute and low outcomes, with a P-value of 0.943 (Table 1). Additionally, oxygen saturation was defined as less than 94% (5,9,12). the extracted outcomes were presented by age and gen- Comorbidities were classified based on the International Classification of Diseases, Revision 10 (ICD-10) diagnostic der (Figure 2). codes, then we reported any comorbidity, one or more Comorbidities were seen in a high percentage of cases comorbidity, and two or more comorbidities (8,13). where 29% (n=188 of 648) had one or more. Comorbidities Lymphocytopenia was defined as a lymphocyte count of were higher in the critical group with 42.9% (n=33) having less than 1500 per cubic millimetre (14). one or more comorbidity, and 27.3% (n=21) having two or The primary endpoint of our study was ICU admission, more comorbidities. On the other side, 27.1% (n=155) of the death or recovery. The secondary endpoint was the in- non-critical patients had one or more comorbidity, and hospital length of stay (LOS) in days. Patients included 10% (n=57) had two or more comorbidities. The association in our study were classified into critical and non-critical between the presence of one or more comorbidity was groups. Critical cases were defined as patients with ICU significantly associated with outcomes with P=0.004. admission or death. Non-critical cases were defined as The comorbidities included diabetes mellitus (DM), recovered patients with hospital discharge without ICU hypertension (HTN), cardiac diseases, chronic respiratory admission in accordance with MoH coronavirus disease diseases (CRD), cancer, immunodeficiency, and chronic guidelines (15). This study was approved by the MoH kidney diseases (CKD). Institutional Review Board Central Committee (Approval Diabetes was seen in 11.3% (n=73 of 648) of the cases number 20-75 M). Data privacy and confidentiality were with 20.8% (n=16) in the critical arm versus 10% (n=57) maintained throughout the study as subjects were labeled in the non-critical arm (P=0.005). Cardiac and cancer/ with unique identification numbers; data concealment immunodeficient patients were 3.5% (n=23 of 648) and was maintained throughout the study by generating 2.8% (n=18 of 648) of the cases, respectively. Cardiac strong passwords for the electronic system and limiting patients were present in 10.4% (n=8) of the critical group access to designated investigators after signing non- versus 2.6% (n=15) in the non-critical group P=0.001. disclosure agreement forms. Similarly, cancer and immunodeficiency were seen in Descriptive statistics were used to describe categorical 6.5% (n=5) of the critical arm versus 2.3% (n=13) in the variables that were presented by counts and percentages. non-critical arm. Among cases, CRD was reported in In contrast, continuous variables were based on the 12.5% (n=81 of 648) of the population with 22.1% (n=17) in median and interquartile range (IQR) since the normality the critical patients arm versus 11.2% (n=64) in the non-

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Figure 1 Study flowchart for COVID-19 laboratory-confirmed cases with definitive outcomes in Saudi Arabia, 1–31 March, 2020

Non Critical N=571

COVID-19 cases ICU admission and Confirmed COVID-19 with definitive Death N=12 cases N=1519 outcomes N=648

Critical N=77

ICU admission and Excluded Recovery N=65 Active COVID-19 cases N=871

critical arm with statistically significant differences The overall in-hospital length of stay (LOS) in days P=0.007 (Table 1). had a median (IQR) of 5 (14) days. There was a significant Fever was seen in 85.3% (n=163 of 191), with a slightly difference in the LOS P=0.001 as critical patients had higher percentage 94.7% in the critical group (n=36) longer LOS with a median (IQR) of 11.5 (11) days versus 4 (12) days for non-critical cases (Table 1). The LOS was versus 83% (n=127) in the non-critical group. However, illustrated for different risk groups (Figure 3). Older there was no statistical difference across the two groups. patients (age ≥65), diabetic, hypertensive, CKD, and Cough was reported in 89% (n=203 of 228) of the total cancer patients/immunodeficient had a longer median group with a significant difference across the two groups LOS of 10 days. Patients without comorbidities had the outcomes P=0.049. Sore throat, runny nose, and headache lowest median LOS with only two days (Figure 3). were reported in 79.3% (n=115 of 145), 74.5% (n=73 of 98) and 27.8% (n=140 of 503) respectively. None of those Several risk factors were explored using logistic regression with outcomes being binary as critical or non- symptoms showed significant differences across critical critical. Crude and adjusted ORs were calculated using and non-critical arms. Gastrointestinal (GI) symptoms age as a continuous variable and gender (Table 2). Male and myalgia were reported by 14.1% (n=71 of 503) and gender was found to be a statistically significant risk 28.8% (n=145 of 503), respectively. In addition, there were factor P=0.012 with a crude OR and 95% CI of 2.01 (1.22– no statistical differences observed across the two arms 3.34). The OR of male gender became 1.92 (1.15–3.20) after outcomes (Table 1). adjusting for age. Older age was found to be significant Vital signs were evaluated for the population based on the continuous and categorical scales. Those with an on their continuous scale or predefined categories. age of ≥ 65 years had 3.15 (1.40–7.09) higher odds ratios However, for vital signs and laboratory results, there were of experiencing ICU admission or death with significant missing data for a high number of cases. There was no P=0.007. Moreover, age categories showed an increasing statistical difference in both continuous and categorical trend of being in the critical group where the age group presentation where heart rate ≥ 100 beats per minute 41–60 years had an OR=1.90 (0.69–5.25) and those >60 occurred in 36.8% (n=7) of the critical group versus 20.8% years had OR=4.04 (1.32–12.36) against the 1–20 years (n=20) of the non-critical group. Similarly, the respiratory reference group. rate had a median (IQR) of 20 (2) breaths per minute. The Being a smoker had an OR=0.98 (0.51–1.88) with a non- cut-off for the categories was taken as 24 breaths per significant P-value that remained non-significant even minute. No significant difference occurred in the groups’ after adjusting for age and sex. Comorbidities showed outcomes. Oxygen saturation had a median (IQR) of 98 (3) significantly increased odds of being in the critical group % with a cut-off value of 94%. The comparison across the with one or more comorbidity having OR=2.01 (1.24– two groups outcomes yielded no significant differences 3.28), two or more comorbidities had OR=3.38 (1.91–5.99), either. Finally, systolic and diastolic blood pressures had DM 2.37 (1.28–4.37), and HTN 2.28 (1.23–4.20). These a median (IQR) of 125 (22) mmHg and 74 (12) mmHg, comorbidities had their adjusted OR decreased indicating respectively, with no significant differences in the critical that the age and gender are potential confounders. versus non-critical groups (Table 1). Neutrophils as well Patients with CKD had an OR=1.50 (0.32–6.96) that as WBC total count and lymphocytes percentages had no remained non-significant when adjusted for age and statistically significant differences across the groups of sex. On the other hand, CRD was considered to be a these variables (Table 1). significant risk factor with an adjusted OR=2.29 (1.24–

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Table 1 Baseline characteristics of the COVID-19 cases based on their reported outcomes

Characteristic Total Patients Critical Non-critical P-value* (N=648) (N=77) (N=571) Sex* 0.006 Male 342 (52.8%) 52 (67.5%) 290 (50.8%) Female 306 (47.2%) 25 (32.5%) 281 (49.2%) Age* (MD, IQR) -years 34 (19) 37 (27) 33 (18) 0.001 Age* Categories -years 0.001 1-20 69 (10.6%) 5 (6.5%) 64 (11.2%) 21-40 359 (55.4%) 38 (49.4%) 321 (56.2%) 41-60 170 (26.2%) 22 (28.6%) 148 (25.9%) >60 50 (7.7%) 12 (15.6%) 38 (6.7%) Age* (binary) -years 0.001 <65 616 (95.1%) 68 (88.3%) 548 (96.0%) ≥65 32 (4.9%) 9 (11.7%) 23 (4.0%) Smoking Status (N=647) 0.943 Yes 104 (16.1%) 12 (15.8%) 92 (16.1%) No 543 (83.9%) 64 (84.2%) 479 (83.9%) Occupation 0.443 Working in health care facilities × 101 (15.6%) 14 (18.2%) 87 (15.2%) Military 21 (3.2%) 4 (5.2%) 17 (3.0%) Others 526 (81.2%) 59 (76.6%) 467 (81.8%) Comorbidities Diabetes Mellitus* 73 (11.3%) 16 (20.8%) 57 (10.0%) 0.005 Hypertension* 75 (11.6%) 16 (20.8%) 59 (10.3%) 0.007 Chronic kidney disease 12 (1.9%) 2 (2.6%) 10 (1.8%) 0.605 Chronic respiratory diseases*‡ 81 (12.5%) 17 (22.1%) 64 (11.2%) 0.007 Cancer/Immunodeficiency* 18 (2.8%) 5 (6.5%) 13 (2.3%) 0.035 Cardiac diseases* † 23 (3.5%) 8 (10.4%) 15 (2.6%) 0.001 No comorbidity 382 (59.0%) 23 (29.8%) 359 (62.9%) 0.001 1 or more Comorbidity* 188 (29.0%) 33 (42.9%) 155 (27.1%) 0.004 2 or more Comorbidity* 78 (12.0%) 21 (27.3%) 57 (10.0%) 0.001 Length of stay* (MD, IQR) -days 5 (14) 11.5 (11) 4 (12) 0.001 Symptoms Fever (N=191) 163 (85.3%) 36 (94.7%) 127 (83.0%) 0.067 Cough* (N=228) 203 (89.0%) 41 (97.6%) 162 (87.1%) 0.049 Sore Throat (N=145) 115 (79.3%) 18 (85.7%) 97 (78.2%) 0.433 Runny Nose (N=98) 73 (74.5%) 7 (63.6%) 66 (75.9%) 0.381 Headache (N=504) 140 (27.8%) 10 (18.2%) 130 (29.0%) 0.092 GI Symptoms ǂ (N=504) 71 (14.1%) 11 (20.0%) 60 (13.4%) 0.182 Myalgia (N=504) 145 (28.8%) 17 (30.9%) 128 (28.5%) 0.710 Vital Signs Temperature (N=268) -֯C 0.132 <38 219 (81.7%) 34 (73.9%) 185 (83.3%) ≥38 49 (18.3%) 12 (26.1%) 37 (16.7%) Heart rate (N=115) -beats/min 0.133 <100 88 (76.5%) 12 (63.2%) 76 (79.2%) ≥100 27 (23.5%) 7 (36.8%) 20 (20.8%) Respiratory rate (MD, IQR) - breaths/min 20 (2.0) 20 (4.0) 20 (2.0) 0.260 Respiratory rate (N=106) 0.187 ≤24 101 (95.3%) 17 (89.5%) 84 (96.6%) > 24 5 (4.7%) 2 (10.5%) 3 (3.4%)

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Table 1 Baseline characteristics of the COVID-19 cases based on their reported outcomes (concluded)

Characteristic Total Patients Critical Non-critical P-value* (N=648) (N=77) (N=571) SBP (MD, IQR) -mmHg 125 (22.0) 121 (20.0) 125 (21.0) 0.336 DBP (MD, IQR) -mmHg 74 (12.0) 74 (10.0) 74.5 (14.0) 0.450 Oxygen saturation (MD, IQR) -% 98 (3.0) 98 (3.3) 98 (3.0) 0.659 Oxygen saturation (N=259) 0.610 < 94 28 (10.8%) 4 (8.7%) 24 (11.3%) ≥94 231 (89.2%) 42 (91.3%) 189 (88.7%) Blood Laboratory testing WBC means (MD, IQR) -103 /µL 5.5 (3.3) 6.5 (7.8) 5.5 (3.0) 0.460 WBC (N=34) 0.906 <4 5 (14.7%) 1 (12.5%) 4 (15.4%) 4-12 26 (76.5%) 6 (75.0%) 20 (76.9%) >12 3 (8.8%) 1 (12.5%) 2 (7.7%) Neutrophils (MD, IQR) -% 62.1 (67.9) 68 (47.3) 60.2 (67.3) 0.405 Neutrophils (N=28) 0.777 <55 10 (35.7%) 2 (28.6%) 8 (38.1%) 55-70 9 (32.1%) 2 (28.6%) 7 (33.3%) >70 9 (32.1%) 3 (42.9%) 6 (28.6%) Lymphocytes (MD, IQR) -% 21.8 (13.7) 22.4 (31.2) 21.8 (13.0) 0.919 Lymphocytes (N=23) 0.923 <20 10 (43.5%) 3 (50.0%) 7 (41.2%) 20-40 10 (43.5%) 2 (33.3%) 8 (47.1%) >40 3 (13.0%) 1 (16.7%) 2 (11.8%) MD=median; IQR=interquartile range; GI=gastrointestinal; SBP=systolic blood pressure; DBP=diastolic blood pressure; WBC=white blood cells * Significant result atɑ =0.05 × Involves physicians, nurses, pharmacists, lab technicians, cleaners, and other workers in health care facilities ‡ Includes asthma, COPD, interstitial lung disease, bronchiectasis, lung cancer, and others † Includes Ischemic heart diseases and heart failure ǂ Involves abdominal pain, vomiting, or diarrhoea

4.25). Cancer/immunodeficient patients had a significant more in the critical group 67.5% versus 32.5% in females. crude OR=2.98 (1.03–8.61) that became non-significant These findings are consistent with previous evidence when adjusted with OR=2.24 (0.73–6.87). Finally, cardiac that suggests male patients have a higher severity and patients showed the highest OR=4.30 (1.76–10.50) that mortality (6,16). remained significant even after adjusting for age and The median age of our sample was 34 years; this could sex with an OR=3.05 (1.16–8.02). None of the symptoms be attributed to the young population of Saudi Arabia showed a significant association with the outcomes even (17). When age was analyzed as a continuous variable, after adjusting for age and sex (Table 2). it showed a significant association with increased risk by almost 3% each year. Consistent with the literature, Discussion cases aged 65 years or older had an increased risk of being admitted to ICU or dying from COVID-19 (18,19). To the best of our knowledge, this is one of the first The results were also significant in patients older than studies in the Eastern Mediterranean Region to assess 60 years of age with an increase in risk by 3.65 times the association between common comorbidities, clinical (95% CI: 1.18–11.27) in relation to those 1–20 years-old manifestations and laboratory results for critical COV- cases. Remarkably, 15.6% of the critical cases were over ID-19 patients. We found an association between gender, the age of 60. These findings confirmed the previous age, diabetes, HTN, chronic respiratory diseases, cardiac evidence reporting age as a risk factor for poor outcomes diseases, cancer patients/immunodeficiency with the (5,20). However, with a lower cutoff age of 60 years outcomes of clinical interest. There was no significant as- when compared with recent studies (2,18). This might sociation among tobacco smokers or patients presenting be related to comorbidities appearing at an early age in with specific signs and symptoms. our population (21). Age-related responses with weak The gender distribution of our patients was 53% immune systems are probable contributing factors for males and 47% females. In addition, males were seen adverse outcomes of the disease (18).

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Figure 2 Age and gender distribution per outcomes in 648 laboratory-confirmed COVID-19 cases with definitive outcomes in Saudi Arabia, 1–31 March, 2020

Male Female >60

41-60

21-40 Age in years

1-20 Non-critical Critical 200 150 100 50 0 50 100 150 200 Number of Patients

Both DM and HTN were associated with worse with worse outcomes among COVID-19 patients (5,6). outcomes with a crude OR around 2.37 and 2.28, The impact of cardiovascular diseases in COVID-19 could respectively. This is supported by previous cohort studies be related to the impaired cardiovascular compensatory confirming similar findings (5,6). However, the adjusted mechanism or the direct cardiac injury reported to be OR became non-significant (P = 0.304, P = 0.443 for DM associated with a higher incidence of worse outcomes and HTN, respectively), which may indicate that the (22). Furthermore, a study conducted in Wuhan, China, crude OR was biased. On the other hand, patients with found cardiac injuries in almost 20% of their COVID-19 a history of cardiac diseases had significantly higher patients and more frequent in cardiac patients with adjusted OR, strongly suggesting that cardiac diseases higher mortality (23). In our study, CRD was a significant were an independent risk factor for ICU admission factor for ICU admission and mortality as adjusted with and mortality. This concurs with findings reported by an OR of 2.29 (CI: 1.24–4.25) and P = 0.008. This was previous studies that cardiac diseases were associated supported by similar findings from a recent observational

Figure 3 Median length of in-hospital stay (LOS) for a total of 648 COVID-19 patients according to different risk factors and outcomes

According to Risk Factors CKD 10 HTN 10 DM 10 Cancer/Immodeﬁciency 10 Age≥65 10 Patients ≥1 comorbidity 9 Patients ≥2 comorbidity 9 Cardiac diseases 9 CRD 7 Smoking 5 Age<65 4 Patients without comorbidity 2 According to Outcomes Critical 11.5 Non-critical 4 0 2 4 6 8 10 12 Median LOSLOS(Days) (days)

CKD=chronic kidney diseases; HTN=hypertension; DM=diabetes mellitus; CRD=chronic respiratory diseases

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Table 2 Risk factors associated with intensive care unit (ICU) admission or death among COVID-19 patients

Crude OR (95% CI) P-value Adjusted OR* (95%CI) P-value Sex (Male) 2.01 (1.22-3.34) 0.006 1.92 (1.15-3.20) 0.012 Age (continuous) -years 1.03 (1.01-1.05) 0.001 1.03 (1.01-1.04) 0.001 Age (≥65) - years 3.15 (1.40-7.09) 0.005 3.07 (1.35-6.96) 0.007 Age Categories - years 1-20 Reference - Reference 21-40 1.52 (0.57-3.99) 0.401 1.33 (0.50-3.55) 0.564 41-60 1.90 (0.69-5.25) 0.214 1.63 (0.59-4.54) 0.35 >60 4.04 (1.32-12.36) 0.014 3.65 (1.18-11.27) 0.024 Smoker 0.98 (0.51-1.88) 0.943 0.79 (0.40-1.58) 0.517 Comorbidities One or more comorbidity 2.01 (1.24-3.28) 0.005 1.51 (0.87-2.62) 0.141 Two or more Comorbidity 3.38 (1.91-5.99) 0.001 2.57 (1.33-4.97) 0.005 Diabetes Mellitus 2.37 (1.28-4.37) 0.006 1.45 (0.72-2.93) 0.304 Hypertension 2.28 (1.23-4.20) 0.009 1.37 (0.64-2.80) 0.443 CRD 2.25 (1.23-4.08) 0.008 2.29 (1.24-4.25) 0.008 Chronic Kidney diseases 1.50 (0.32-6.96) 0.608 0.98 (0.21-4.68) 0.981 Cardiac Diseases 4.30 (1.76-10.50) 0.001 3.05 (1.16-8.02) 0.024 Cancer/Immunodeficiency 2.98 (1.03-8.61) 0.043 2.24 (0.73-6.87) 0.158 Symptoms Fever 3.69 (0.84-16.27) 0.085 2.78 (0.61-12.59) 0.185 Cough 6.07 (0.79-46.23) 0.081 5.05 (0.65-39.02) 0.121 Sore Throat 1.67 (0.46-6.09) 0.437 1.28 (0.34-4.88) 0.715 Runny Nose 0.56 (0.15-2.09) 0.386 0.50 (0.13-1.94) 0.317 Headache 0.55 (0.27-1.12) 0.096 0.62 (0.30-1.28) 0.199 GI Symptoms 1.62 (0.79-3.31) 0.185 1.80 (0.87-3.74) 0.113 Myalgia 1.12 (0.61-2.06) 0.711 1.18 (0.63-2.18) 0.610 Vital Signs Temperature (≥38) -֯C 1.77 (0.84-3.72) 0.136 1.64 (0.77-3.51) 0.200 Heart Rate ≥100 -beats/min 2.22 (0.77-6.36) 0.139 1.99 (0.67-5.88) 0.216 Respiratory Rate (Continuous) -breaths/min 1.13 (0.93-1.36) 0.212 1.10 (0.91-1.33) 0.307 Respiratory rate (>24) 3.29 (0.51-21.24) 0.210 2.34 (0.35-15.84) 0.384 SBP (continuous) -mmHg 0.99 (0.96-1.02) 0.595 0.99 (0.96-1.02) 0.365 DBP (continuous) -mmHg 0.97 (0.93-1.03) 0.319 0.96 (0.90-1.02) 0.143 Oxygen saturation % 1.02 (0.93-1.13) 0.652 1.04 (0.93-1.15) 0.513 Oxygen saturation (< 94) 0.75 (0.25-2.28) 0.611 0.75 (0.24-2.33) 0.623 OR=odds ratio; CI=confidence interval CRD=chronic respiratory diseases; GI=gastrointestinal; SBP=systolic blood pressure; DBP=diastolic blood pressure * Adjusted for age and gender study carried out in the UK indicating that CRD was a outcomes for COVID-19 patients because the disease risk factor for in-hospital mortality in COVID-19 patients might have an unpredictable course. (6). The missing data variables in our study contributed Having two or more comorbidities are independent broadly to these differences in that we retrieved only 5.2% risk factors for ICU admission and mortality with an of WBCs, 4.3% of neutrophils, and 3.5% of lymphocytes adjusted OR=2.57. Comorbidities should be considered results; these failed to generate a robust analysis to assess when risk stratifying patients with COVID-19 as the association. supported by the nationwide analysis from China (8). Tobacco smoking is a controversial factor in Although initial symptoms and vital signs were not COVID-19. There has been a strong relation between associated with worse outcomes, it is crucial to not fully angiotensin-converting enzyme 2 (ACE2) expression rely on the initial clinical manifestations in predicting in the lung tissue and the spread of COVID-19 disease.

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Smoking is remarkably associated with dose-dependent assessment tool that contains clinical symptoms, risk upregulation of ACE2 expression causing more harm in factors, radiological features, and laboratory findings developing critical outcomes among the patients (24,25). of COVID-19 patients to anticipate the clinical courses On the contrary, some reports have not found smoking to and guide future management. Although some of the be associated with COVID-19 severity (26). Surprisingly, essential risk factors associated with poor outcomes have one paper proposed smoking to be a protective factor been described in this study, further prospective studies against COVID-19 in developing less serious infections in the region are recommended to investigate various and hypothesized the pathophysiological explanation radiological features and expected laboratory values as could be related to the nicotine effect (27). Nevertheless, predictors of COVID-19 prognosis. our result confirmed the poor association between smoking and worse outcomes encouraging more This study identified many risk factors associated structured studies in that subject to provide conclusive with adverse outcomes in COVID-19 patients, but several evidence. limitations were present. First, due to the retrospective nature of this study, we could not eliminate missing Remarkably, the median LOS was 11.5 days for critical variables especially, in the vital signs and laboratory COVID-19 patients with only four days for the non-critical results. Therefore, no data analysis or interpretation could arm. This was expected considering the severity of the disease and the associated comorbidity; patients without be withdrawn from these variables. Second, radiological comorbidities had a span of two days while those with studies were not available in the HESN database. This comorbidities had a span of nine days. A recent study would have an additive value in risk-stratifying patients in China reported a median LOS of 14.5 days for critical based on their radiological abnormalities. Third, many patients, higher than the LOS seen in our results. This laboratory results were not retrieved including renal could be explained by their higher median age of critical function tests, liver function tests, D-dimer, coagulation cases compared to our cases, 63 years versus 37 years profile, and troponin levels. These could guide clinical respectively (14). practice if correlated with COVID-19 disease severity and A better understanding of this disease is critical related outcomes. to reducing the impact of the pandemic. Many of our findings are concordant with reported risk factors for Conclusions COVID-19 disease. In many ways, this study will help risk-stratify, prioritize the detection, and guide clinical In subjects with COVID-19, age, male gender, cardiac dis- management and disposition effectively based on their eases, CRD, and having two or more comorbidities were demographic data, clinical symptoms, and associated independent risk factors for ICU admission and mortali- comorbidities. Furthermore, it will support decision- ty. Although the young Saudi population has limited risk, makers to unify clinical guidelines and describe we found that age more than 60 years was associated predictors for mortality of COVID-19 in the Eastern with worse outcomes. Finally, neither the initial sign and Mediterranean Region. Based on the current evidence of symptoms nor tobacco smoking were linked to adverse risk factors and predictors, we suggest designing a special outcomes. Based on the current evidence of risk factors multi-item scale system to prognosticate COVID-19 and predictors, we suggest designing a unique mul- patients. We encourage designing a comprehensive ti-item scale system to prognosticate COVID-19 patients.

Acknowledgment We would like to acknowledge the contribution of all MoH staff, mainly the General Directorate of Statistics and Infor- mation Management, and Directorate General of Infectious Diseases. Funding: None. Competing interests: None declared.

Facteurs de risque associés à une détérioration des résultats pour la COVID-19 : étude rétrospective en Arabie saoudite Résumé Contexte : L’ émergence rapide de la maladie à nouveau coronavirus 2019 (COVID-19) a entraîné l’infection de millions de patients et des centaines de milliers de décès dans le monde entier. La prestation des services de soins de santé est mise à mal en raison de l’augmentation massive du nombre de patients infectés pendant cette pandémie. Objectifs : La présente étude visait à évaluer les facteurs de risque associés à un mauvais pronostic chez les patients atteints de COVID-19 en Arabie saoudite.

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Méthodes : Il s’agissait d’une étude de cohorte rétrospective multicentrique qui incluait tous les cas de COVID-19 confirmés en laboratoire, avec des résultats définitifs en Arabie saoudite en mars 2020. Les données démographiques, les antécédents cliniques, la comorbidité et les résultats ont été extraits de la base de données du National Health Electronic Surveillance Network. Nous avons utilisé des modèles de régression logistique pour calculer les odds ratios bruts et ajustés (OR) afin d’étudier les facteurs de risque pour les résultats critiques (admission en unité de soins intensifs ou décès) parmi les cas de COVID-19. Résultats : Nous avons inclus 648 patients positifs pour la COVID-19, dont l’âge médian était de 34 ans. Parmi eux, 11,9 % appartenaient au groupe critique. Les facteurs de risque associés aux pires résultats comprenaient l’appartenance au sexe masculin (OR = 1,92), un âge supérieur à 60 ans (OR = 3,65), les maladies cardiaques (OR = 3,05), les maladies respiratoires chroniques (OR = 2,29) et les cas présentant deux comorbidités ou plus (OR = 2,57) après ajustement en fonction de l’âge et du sexe ; tous avaient des valeurs p inférieures à 0,05 significatives. Conclusions : Les facteurs de risque indépendants pour les résultats critiques parmi les cas de COVID-19 comprennent la vieillesse, l’appartenance au sexe masculin, les maladies cardiaques, les maladies respiratoires chroniques et la présence de deux comorbidités ou plus. Nous recommandons de mettre au point un système d’échelle unique multi-items pour pronostiquer les patients atteints de COVID-19.

عوامل اخلطر املرتبطة بالنتائج السيئة ملرض كوفيد- : 19دراسة بأثر رجعي يف اململكة العربية السعودية أنس خان، صقر الثنيان، يوسف الصفيان، رائد العتيبي، عبد اهلل مبارك، حممد عرفات، عبد اهلل عسريي، هاين جوخدار اخلالصة اخللفية: أدى االنتشار الرسيع لفريوس كورونا املستجد 2019 )كوفيد- (إىل 19إصابة املاليني من املرىض ووقوع مئات اآلالف من الوفيات يف مجيع أنحاء العامل. فقد تأثرت خدمات الرعاية الصحية املقدمة ًسلبا ًنظرا لالزدياد املفاجئ يف أعداد املرىض املصابني خالل اجلائحة. األهداف: هدفت هذه الدراسة إىل تقييم عوامل اخلطر املرتبطة بالنتائج السيئة ملرىض كوفيد-19 يف اململكة العربية السعودية. طرق البحث:أجرينا دراسة حشدية رجعية متعددة املراكز شملت مجيع حاالت كوفيد-19 املؤكدة نتائجهم بالتحاليل املخربية وهلم نتائج هنائية خالل شهر مارس/ آذار يف اململكة العربية السعودية. وتم مجع البيانات السكانية والتاريخ اإلكلينيكي واألمراض املصاحبة والنتائج من قاعدة بيانات النظام اإللكرتوين للرتصد الوبائي )حصن(. وتم استخدام نامذج االنحدار اللوجيستي حلساب نسب األرجحية اخلام ّواملعدلة الستكشاف عوامل اخلطر املصاحبة للنتائج احلرجة حلاالت كوفيد-19 )التنويم يف وحدة العناية املركزة أو الوفاة(. النتائج: تضمنت الدراسة 648 ًمريضا ًإجيابيا بكوفيد- 19بمتوسط أعامر 34 ًعاما. منهم % يف11.9 املجموعة احلرجة. وشملت عوامل اخلطر > املرتبطة بالنتائج السيئة الذكور )نسبة األرجحية=1.92(، العمر 60 ًعاما )نسبة األرجحية=3.65(، أمراض القلب )نسبة األرجحية=3.05(، األمراض التنفسية املزمنة )نسبة األرجحية= (، 2.29واحلاالت املصابة املرتبطة بمرضني مصاحبني أو أكثر )نسبة األرجحية=2.57( بعد تعديل العمر واجلنس؛ وكانت القيمة االحتاملية لكل منهم ذات أمهية إحصائية > 0.05. االستنتاجات: تشمل عوامل اخلطر املستقلة املرتبطة بالنتائج احلرجة ملرىض كوفيد-19: التقدم يف السن والذكور ومرىض القلب واألمراض التنفسية املزمنة واحلاالت املصابة املرتبطة بمرضني مصاحبني أو أكثر. ونويص بتصميم نظام مقياس فريد متعدد العنارص للتنبؤ باحلالة الصحية ملرىض كوفيد19-.

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7. Wu Z, McGoogan J. characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) Outbreak in China. JAMA. 2020;323 (13):1239-1242. https://doi:10.1001/jama.2020.2648. 8. Guan W, Liang W, Zhao Y, Liang H, Chen Z, Li Y, et al. Comorbidity and its impact on 1590 patients with Covid-19 in China: A nationwide analysis. Eur Respir J. 2020;55 (6):2000547. https://doi.org/10.1183/13993003.00547-2020. 9. Alsofayan Y, Althunayyan S, Khan A, Hakawi A, Assiri A. Clinical characteristic of COVID-19 in Saudi Arabia: A national retrospective study. J Infect Public Health. 2020;13(7):920-925.https://doi.org/10.1016/j.jiph.2020.05.026. 10. National laboratories. Geneva: World Health Organization; 2020 (https://www.who.int/emergencies/diseases/novel-coronavi-� rus-2019/technical-guidance/laboratory-guidance/, accessed 8 June 2020). 11. Risk stratification for severe disease in patients with coronavirus disease 2019 (COVID-19). UpToDate; 2020https://www.upto -� date.com/contents/image/print?imageKey=PWYS%2F127891&topicKey=PC%2F127759&search=covid&source=outline_link&se- lectedTitle=5~150, accessed 1 June 2020). 12. Singer M, Deutschman C, Seymour C, Shankar-Hari M, Annane D, Bauer M, et al. The Third International Consensus Defini- tions for Sepsis and Septic Shock (Sepsis-3). JAMA. 2016;315 (8):801-810. https://doi:10.1001/jama.2016.0287. 13. ICD-10 for Mortality and Morbidity Statistics. Geneva: World Health Organization; 2019 (https://icd.who.int/browse10/2019/en, accessed 24 May 2020). 14. Guan W, Ni Z, Hu Y, Liang W, Ou C, He J, et al. Clinical characteristics of coronavirus disease 2019 in China. New Engl J Med. 2020;382 (18):1708-1720. https://doi:10.1056/NEJMoa2002032. 15. COVID-19 coronavirus disease guidelines. Riyadh: Ministry of Health; 2020 (https://www.moh.gov.sa/Ministry/MediaCenter/ Publications/Documents/Coronavirus-Disease-2019-Guidelines-v1.2.pdf, accessed 28 May 2020). 16. Chen T, Wu D, Chen H, Yan W, Yang D, Chen G, et al. Clinical characteristics of 113 deceased patients with coronavirus disease 2019: retrospective study. BMJ. 2020;368:m1091. https://doi.org/10.1136/bmj.m1091. 17. Population by gender, age groups and nationality (Saudi/Non-Saudi). Riyadh: General Authority for Statistics; 2018 (https:// www.stats.gov.sa/en/5680/, accessed 27 May 2020). 18. Wu C, Chen X, Cai Y, Xia J, Zhou X, Xu S, et al. Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China. JAMA Intern Med. 2020;180(7):934-943. https://doi. org/10.1001/jamainternmed.2020.0994. 19. Yang X, Yu Y, Xu J, Shu H, Xia J, Liu H, et al. Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study. Lancet Respir Med. 2020 May;8(5):475-481. https:// doi:10.1016/S2213-2600 (20)30079-5. 20. Grasselli G, Zangrillo A, Zanella A, Antonelli M, Cabrini L, Castelli A, et al. Baseline characteristics and outcomes of 1591 patients infected with SARS-CoV-2 admitted to ICUs of the Lombardy region, Italy. JAMA. 2020;323 (16):1574–1581. https://doi:10.1001/ jama.2020.5394. 21. Khoja AT, Aljawadi MH, Al-Shammari SA, Mohamed AG, Al-Manaa HA, Morlock L, et al. The health of Saudi older adults; results from the Saudi National Survey for elderly health (SNSEH) 2006–2015. Saudi Pharm J. 2018 Feb 1;26(2):292-300. https://doi. org/10.1016/j.jsps.2017.11.008. 22. Li B, Yang J, Zhao F, Zhi L, Wang X, Liu L, et al. Prevalence and impact of cardiovascular metabolic diseases on COVID-19 in China. Clin Res Cardiol. 2020;531–538. https://doi.org/10.1007/s00392-020-01626-9. 23. Shi S, Qin M, Shen B, Cai Y, Liu T, Yang F, et al. Association of cardiac injury with mortality in hospitalized patients with COV- ID-19 in Wuhan, China. JAMA Cardiol. 2020;5(7):802-810. https://doi:10.1001/jamacardio.2020.0950. 24. Smith JC, Sausville EL, Girish V, Yuan ML, Vasudevan A, John KM, et al. Cigarette smoke exposure and inflammatory signaling increase the expression of the SARS-CoV-2 receptor ACE2 in the respiratory tract. Dev Cell. 2020 May 16;53(5):514-529.e3. https:// doi.org/10.1016/j.devcel.2020.05.012. 25. Zheng Z, Peng F, Xu B, Zhao J, Liu H, Peng J, et al. Risk factors of critical & mortal COVID-19 cases: A systematic literature review and meta-analysis. J Infect. 2020 Aug;81(2):e16-e25 Epub 2020 https://doi.org/10.1016/j.jinf.2020.04.021. 26. Lippi G, Henry BM. Active smoking is not associated with severity of coronavirus disease 2019 (COVID-19). Eur J Intern Med. 2020 May;75:107-108. https://doi:10.1016/j.ejim.2020.03.014. 27. Miyara M, Tubach F, Pourcher V, Morelot-Panzini C, Pernet J, Haroche J, et al. Low rate of daily active tobacco smoking in patients with symptomatic COVID-19. Qeios. 2020. https://doi:10.32388/WPP19W.4.

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Quality utilization of antenatal care and low birth weight: evidence from 18 demographic health surveys

Saverio Bellizzi1 and Susanna Padrini2

1Partnership for Maternal, Newborn and Child Health, Geneva, Switzerland (Correspondence to: S. Bellizzi: [email protected]). 2Associazione Italiana per la Solidarietà tra i Popoli (AISPO), Milano, Italy.

Abstract Background: Low birthweight is a crucial factor in child mortality and morbidity and affects almost 20% of infants worldwide, mostly in low- and middle-income countries. Aims: To assess the relationship between access to and quality of antenatal care and occurrence of low birth weight. Methods: We analysed data from 18 demographic and health surveys, from 2005 to 2013, including 69 446 children. The main study outcome was birthweight < 2.5 kg, and access to and number of antematal care visits were exposure variables. Moreover, antenatal care attendants and time of visit (trimester) were considered. Multiple logistic regression adjusted for sampling at primary and country level was utilized. Results: At least 1 and ≥ 4 antenatal care consultations were both associated with decreased odds of low birth weight when compared to none and < 4 antenatal care consultations, respectively. Additional benefit stemmed from having skilled antenatal care attendants and the first antenatal care consultation during the first trimester. Conclusions: Proper antenatal care coverage during pregnancy is beneficial for preventing low birth weight in low- and middle-income countries. Keywords: antenatal care, demographic health survey, low birth weight, low-income country, middle-income country Citation: Bellizzi S; Padrini S. Quality utilization of antenatal care and low birth weight: evidence from 18 demographic health surveys. East Mediterr Health J. 2020;26(11):1381-1387. https://doi.org/10.26719/emhj.20.055 Received: 14/11/18; accepted: 24/11/19 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 countries. Some studies have shown that ANC improves birthweight (17,18), while others have shown a lack of In 2012, the World Health Assembly endorsed a compre- evidence for the effectiveness of content, frequency hensive plan under Resolution 65.6 with specific global nutrition targets for 2025 (1). This policy included a 30% and timing of visits in standard ANC programmes on reduction in low birthweight (LBW) (2), corresponding maternal and child health (19). to a reduction from 20 million to ~14 million neonates Our research used data from demographic and with birthweight < 2.5 kg (3) between 2012 and 2025. health surveys (DHSs) in 18 countries and examined the LBW affects almost one sixth of infants worldwide with association between adequate utilization of ANC and > 95% of cases located in developing countries (3), and is occurrence of LBW. recognized as 1 of the most influential factors on child mortality and morbidity. LBW increases mortality risk by 20–30 times (4), and contributes to 60–80% of all ne- Methods onatal deaths worldwide (5,6). Surviving infants are at Study design higher risk of pathological conditions such as infection immediately after birth and throughout the first year of This was a population-based study of data from 18 DHSs life (7). LBW is also associated with morbidity later in life, between 2005 and 2013, which reported birthweight for at such as psychosocial disorders (8), impaired cognitive least 80% of births over the 5 years preceding the survey: function (9), coronary heart disease (10) and noninsulin Albania 2008/2009, Armenia 2010, Congo (Brazzaville) dependent diabetes (11). Several risk factors are claimed 2011/2012, Dominican Republic 2013, Gabon 2012, Guyana to be associated with LBW, including maternal factors, 2009, Honduras 2011/2012, Indonesia 2012, Jordan 2012, pregnancy, multiple gestation, socioeconomic character- Kyrgyzstan 2012, Maldives 2009, Republic of Moldova istics, drug treatment and body mass index (12–15). 2005, Peru 2012, Philippines 2013, Sao Tome and Princi- At least 4 antenatal care (ANC) consultations, with pe 2008/2009, Swaziland 2006/07, Tajikistan 2012, and the first preferably in the first trimester (16), has been a Ukraine 2007. Detailed information on procedures and worldwide recommended policy for the last 2 decades. sampling techniques for all DHSs have been published However, there is still inconclusive evidence on its elsewhere (20). Face-to-face interviews were carried out impact on maternal and neonatal outcomes in developing for a total of 213 752 women.

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Study population each country and the Institutional Review Board of ORC Macro approved the DHS data collection procedures. The study population consisted of all the latest singleton live births (n = 77 809) during the 5 years preceding the DHS in each country. After excluding 8363 (10.7%) indi- Results viduals for whom we had missing data on BW, the final Overall, 6238 (9.0%) newborns with LBW were record- sample included 69 446 babies. Information on BW was ed, ranging from a minimum of 36 (2.8%) of 1281 in Al- obtained through birth certificates and maternal recall bania to a maximum of 883 (20.8%) of 4238 newborns in for 21 334 (30.7%) and 48 112 (69.3%) infants, respectively. the Philippines (Table 1). Data on ANC were missing for Outcome, exposure and control variables 1404 individuals, corresponding to 2% of the total study population. Most mothers had ANC (n = 66 513; 97.7%) The main outcome was LBW, which was defined as < 2.5 and half of them (n = 33 038) had the first consultation kg. Characteristics of ANC were the exposure variables, during the first trimester (Table 2). Only 6517 (10%) wom- which were defined as follows: “ANC”, if any ANC con- en had < 4 consultations. Almost all pregnant women sultation was performed; “provider”, classified as skilled (97.2%) consulted a trained operator. Less than half of (doctors, nurses or other trained attendants) or unskilled them (n = 31 372) had a good quality of ANC according to attendant (traditional attendants or others); “number of World Health Organization (WHO) criteria. ANC consultations”, subdivided into < 4 or ≥ 4 ANC vis- Table 3 shows a clear trend toward increasing its; “ANC timing”, dichotomized into ANC first consulta- prevalence of LBW with decreasing wealth, poorer tion in the first trimester or after the first trimester; and education and shorter birth intervals, in addition to “quality of ANC”, with ≥ 4 ANC consultations started in higher risk in unwanted pregnancies and female sex. the first trimester with a skilled attendant on 1 side, and There were associations between wealth status and all the others on the other side. A series of socioeconom- education and the quality of ANC. The richest and most ic, pregnancy and maternal characteristics were evalu- educated women, in addition to those living in urban ated as possible confounders, including age, education, areas, were more likely to have ≥ 4 ANC consultations wealth, place of residence, birth interval, birth order, performed by skilled attendants, with the first wanted pregnancy and child sex. consultation during the first trimester. Statistical analysis The adjusted logistic regression showed a significant benefit of having any ANC consultation when compared Statistical analysis was performed using STATA 13.1 SE (StataCorp, College Station, TX, USA). The “svy” command was used to adjust for clustering by primary sam- Table 1 Numbers of live births and low birth weight infants in pling unit. Number of total livebirths and LBW by coun- 18 low- and middle-income countries try were tabulated with relative percentages. All the study categorical confounding variables were tested against Country, year Live births Low birth weight (%) LBW using the χ2 test. Furthermore, we used the χ2 test to examine the association between the quality of ANC Albania 2008/2009 1281 36 (2.8) and the following socioeconomic variables: wealth sta- Armenia 2010 1139 1,438 (6.0) tus, maternal age and education, and place of residence. Congo (Brazzaville 2011/2012) 5355 467 (8.7) The Metaprop syntax (21) was used in the pooled Dominican Republic 2013 2847 378 (13.3) meta-analysis of all country datasets, which generated Gabon 2012 3485 445 (12.8) weighted subgroup and overall pooled estimates with Guyana 2009 1294 167 (12.9) inverse-variance weights obtained from a random-effects Honduras 2011/2012 7062 654 (9.3) model. In this model, no residual heterogeneity was Indonesia 2012 13 045 840 (6.4) assumed. The final model included wealth, age, birth Jordan 2012 6612 817 (12.4) order, birth spacing, education, wanted pregnancy, Kyrgyzstan 2012 3089 147 (4.8) child sex, and rural/urban residence; the factors primary sampling unit and country were added with Maldives 2009 3206 328 (10.2) random effect. Stepwise logistic regression analysis of Republic of Moldova 2005 1350 63 (4.7) LBW on the 5 ANC exposure variables was conducted Peru 2012 7385 479 (6.5) adjusting for socioeconomic, maternal and pregnancy Philippines 2013 4238 883 (20.8) characteristics. P < 0.05 was considered statistically Sao Tome and Principe 2008/2009 1159 79 (6.8) significant. Swaziland 2006/2007 1788 116 (6.5) Ethical approval Tajikistan 2012 2955 197 (6.7) This study used existing data obtained from ORC Mac- Ukraine 2007 2156 74 (3.4) ro (Calverton, MD, USA) through formal request mech- Total 69 446 6238 (9.0) Results are total number of newborns and number of low birthweight infants among the anisms (https://dhsprogram.com). No additional ethical last births for each woman in the preceding 5 years. Results from 18 demographic health review for the secondary analysis was required since surveys.

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Table 2 Distribution of ANC variables among 69 446 low birthweight and normal weight livebirths in 18 low- and middle-income countries in 2005–2013 ANC variables Low birth weight Normal weight P n (%) n (%) χ² ANC No 177 (11.6) 1,352 (88.4) < 0.001 Yes 5948 (8.9) 60 565 (91.1) Time of first ANC consultation First trimester 2795 (8.5) 30 243 (91.5) < 0.001 After first trimester 3248 (9.4) 31 406 (90.6) No. of ANC consultations ≥ 4 5108 (8.5) 54 888 (91.5) < 0.001 < 4 840 (12.9) 5677 (87.1) ANC attendant Skilled 5908 (8.9) 60 291 (91.1) < 0.001 Unskilled 217 (11.8) 1626 (88.2) ANC highest quality Yes 2628 (8.4) 28 744 (91.6) < 0.001 No 3610 (9.5) 34 464 (90.5) ANC = antenatal care. to no ANC (OR 1.2; 95% CI 1.0–1.4) (Table 4). Among nutritional reserves in women with high parity and short infants of women who underwent ANC, having < 4 IPI. consultations, first consultation after the first trimester, Other DHSs from single countries have reported being attended by an unskilled operator and not meeting the benefit of an early start to ANC and the importance WHO quality criteria were associated with 1.5 (95% CI of a sufficient number of consultations. A study from 1.4–1.7), 1.1 (95% CI 1.0–1.2), 1.2 (95% CI 1.1–1.4) and 1.1 (95% Nepal showed how women with no ANC were twice as CI 1.0–1.2) increased ORs of LBW, respectively. likely to have LBW infants when compared to mothers with ≥ 4 ANC consultations (25). A study from Colombia Discussion reported that having the first ANC after the first trimester was associated with an increased OR for LBW This secondary analysis of DHS data from 18 countries when compared with first visits at the first trimester (26). showed that the absence of ANC consultation increased Similar findings were reported in a study in Kenya (27), the risk of LBW. All WHO criteria, separately and com- indicating a positive effect of ANC, which influences bined, for adequate antenatal consultations resulted in dietary behaviour and treatment from any illness that significant protection against LBW. We compared our re- may have negative effects on the health of the fetus. sults on the country incidence of LBW with other sourc- Although our secondary analysis had advantages, es and found no substantial differences. Estimates from such as large sample size and use of standardized the United Nations Children’s Fund and WHO global and questionnaires that limited the risk of intercountry country reports on LBW confirm the smallest percentage variation, it had some limitations. First, we considered (3%) for Albania up to the highest (20%) in the Philippines only the 18 DHSs with at least 80% of data on BW, but (22). we cannot exclude bias for all remaining women not Our findings on the influence of maternal education able to report information, which may have led to on LBW are not surprising. A study in the Islamic Republic underestimation of LBW. Second, two thirds of the of Iran showed that the prevalence of LBW in infants information on BW relied on maternal recall, therefore born to women with no education was 16.9%, which presenting a particular type of misreporting called decreased to 5.4% in women educated to a higher level heaping. Heaping consists of rounding and reporting (23). The explanation may lie in greater access to ANC and weights as multiple of 500 g, which makes interpretation better nutritional behaviour. Similarly, parity and birth difficult when infants are reported as weighing 2.5 kg, and spacing have been detected as important determinants thus likely to be misclassified as having normal weight for LBW. One study showed that mothers with very short (28). Third, several possible confounding variables such interpregnancy intervals (IPIs; < 3 months) and high as genetics and maternal history of diseases were not parity had a higher risk of having LBW infants when available. Finally, we had no information on nutritional compared to those with very short IPI but low parity (24). status of women to exclude maternal factors that would The explanation for these differences may be depleted increase risk of LBW.

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Table 3 Characteristics of mothers of 69 446 low birthweight and normal weight infants in 18 low- and middle-income countries in 2005–2013 Maternal characteristics Low birth weight Normal weight P n (%) n (%) χ² Maternal age (years) 15–19 568 (13.2) 3745 (86.8) < 0.001 20–24 1541 (9.7) 14 305 (90.3) 25–29 1538 (8.1) 17 383 (91.9) 30–34 1155 (7.7) 13 756 (92.2) 35–39 838 (8.5) 8996 (91.5) 40–44 479 (10.4) 4127 (89.6) 45–49 119 (11.7) 896 (88.3) Birth order 1 2,227 (10.6) 19 920 (89.9) < 0.001 > 1 4,011 (8.5) 43 288 (91.5) Preceding birth interval (months) < 18 397 (12.1) 2871 (87.8) < 0.001 18–23 438 (9.2) 4337 (90.8) 24–35 863 (8.4) 9347 (91.5) > 35 2313 (8.0) 26 733 (92.0) Place of residence Urban 2936 (8.7) 30 829 (91.3) 0.01 Rural 3302 (9.2) 32 379 (90.7) Education No education 248 (11.7) 1869 (88.3) < 0.001 Primary 1901 (10.1) 16 897 (89.9) Secondary 3094 (8.7) 32 338 (91.3) Higher 992 (7.6) 12 063 (92.4) Wealth index Poorest 1882 (11.3) 14 780 (88.7) < 0.001 Poorer 1540 (9.4) 14 748 (90.5) Middle 1202 (8.5) 13 009 (91.5) Richer 960 (7.8) 11 378 (92.2) Richest 654 (6.6) 9293 (93.4) Wanted pregnancy Wanted 4077 (8.5) 44 109 (91.5) < 0.001 Not wanted 2156 (10.2) 19 057 (89.8) Child sex Male 2964 (8.2) 33 031 (91.8) < 0.001 Female 3274 (9.8) 30 177 (90.2)

In conclusion, our study reinforces the need to to understand health messages and to be concerned about encourage pregnant women to attend ANC to reduce their health and nutritional status. Poorer women are LBW, with its short- and long-term consequences. Policies less likely to afford the cost of ANC and transportation in areas where health infrastructure is distant. should in particular address access to and quality of ANC among disadvantaged socioeconomic groups, which are Funding: None. at higher risk of LBW. Uneducated mothers are less likely Competing interests: None declared.

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Table 4 Odds ratios for low birthweight in 69 446 singleton births ANC OR (95% CI) unadjusted OR (95% CI) adjusteda No ANC visit 1.3 (1.1–1.6) 1.2 (1.0–1.4) < 4 ANC visits 1.6 (1.5–1.7) 1.5 (1.4–1.7) ANC visit after first trimester 1.1 (1.0–1.2) 1.1 (1.0–1.2) No Skilled ANC 1.4 (1.2–1.6) 1.2 (1.1–1.4) No Quality ANC 1.1 (1.0–1.2) 1.1 (1.0–1.2) aAdjusted for wealth, age, birth order, birth spacing, education, wanted pregnancy, child sex, and rural/urban residence. ANC = antenatal care; CI = confidence interval; OR = odds ratio.

Utilisation qualitative des soins prénatals et faible poids de naissance : données issues de 18 enquêtes démographiques sur la santé Résumé Contexte : Le faible poids à la naissance est un facteur crucial de la mortalité et de la morbidité infantiles et touche près de 20 % des nourrissons dans le monde, principalement dans les pays à revenu faible et intermédiaire. Objectifs : La présente étude avait pour objet d’évaluer le lien entre l’accès aux soins prénatals et leur qualité d’une part, et le faible poids de naissance d’autre part. Méthodes : Nous avons analysé les données de 18 enquêtes démographiques et sanitaires, de 2005 à 2013, portant sur 69 446 enfants. Le principal résultat de l’étude concernait un poids de naissance inférieur à 2,5 kg. L ’ accès aux visites prénatales et le nombre de consultations étaient des variables d’exposition. En outre, le personnel de consultation prénatale et le calendrier des visites (trimestrielles) ont été pris en compte. La régression logistique multiple ajustée pour l ’ échantillonnage aux niveaux primaire et national a été utilisée. Résultats : Deux facteurs, en l’occurrence le fait d’avoir au moins une consultation prénatale et un nombre de visites supérieur ou égal à quatre, ont été associés à une diminution de la probabilité de faible poids de naissance par rapport à l’absence de visite et à un nombre de consultations prénatales inférieur à quatre, respectivement. La mise à disposition de personnel de consultation prénatale qualifié et la première consultation prénatale prévue au cours du premier trimestre de la grossesse constituaient également des avantages. Conclusions : Une couverture adéquate des soins prénatals pendant la grossesse est bénéfique pour prévenir le faible poids de naissance dans les pays à revenu faible et intermédiaire.

عالقة احلصول عىل الرعاية السابقة للوالدة وجودهتا بانخفاض الوزن عند الوالدة: دالئل َمستمدة من 18 ًمسحا ًصحيا ًسكانيا سافرييو بيليزي، سوزانا بادريني اخلالصة اخللفية: ُيعد انخفاض الوزن عند الوالدة أحد العوامل احلاسمة التي قد تؤدي إىل َو َف َيات األطفال واعتالهلم، ّويؤثر عىل ما يقرب من 20٪ من ُالر َّضعيف مجيع أنحاء العامل، ومعظمهم يف البلدان املنخفضة واملتوسطة الدخل. األهداف: هدفت هذه الدراسة إىل تقييم العالقة بني احلصول عىل الرعاية السابقة للوالدة وجودهتا وانخفاض الوزن عند الوالدة. طرق البحث: أجرينا ًحتليال لبيانات َمستمدة من 18 ًمسحا ًصحيا ً وسكانيايف الفرتة من 2005 إىل 2013، شملت 446 69 ًطفال. وكانت نتيجة الدراسة الرئيسية أن الوزن عند الوالدة أقل من كجم، 2.5وكان احلصول عىل الرعاية السابقة للوالدة وعدد الزيارات املتعلقة هبا بمثابة متغريات ُّللتعرض. كام أخذت الدراسة بعني االعتبار أخصائيي الرعاية السابقة للوالدة، ووقت الزيارة )مرحلة احلمل كل ثالثة أشهر(، ُواستخدم انحدار لوجستي متعدد تم تصحيحه ملراعاة أخذ العينات عىل املستويني األويل ُوالق ْطري. النتائج: ارتبط إجراء ما ال يقل عن زيارة طبية واحدة و4 زيارات طبية أو أكثر فيام يتعلق بالرعاية السابقة للوالدة بقلة احتامالت انخفاض الوزن عند الوالدة ًمقارنة بعدم إجراء زيارات طبية وإجراء أقل من 4 زيارات طبية، عىل التوايل. ونشأت فائدة إضافية من ُّتوفر أخصائيني ماهرين يف تقديم الرعاية السابقة للوالدة، وإجراء أول زيارة طبية فيام يتعلق بالرعاية السابقة للوالدة أثناء الثلث األول من احلمل. االستنتاجات: التغطية املناسبة بالرعاية السابقة للوالدة أثناء احلمل مفيدة للوقاية من انخفاض الوزن عند الوالدة يف البلدان املنخفضة واملتوسطة الدخل.

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Macromineral enrichment of white bread reduces postprandial glycaemia without altering sensory properties: a crossover study

Rania El Khoury,1 Noor El Solh,1 Ammar Olabi,1 Imad Toufeili,1 Sani Hlais1 and Omar Obeid1

1Department of Nutrition and Food Science, Faculty of Agricultural and Food Sciences, American University of Beirut, Beirut, Lebanon (Correspondence to: O. Obeid: [email protected]).

Abstract Background: Metabolism of refined carbohydrates, which are associated with detrimental health effects, is known to be affected by macrominerals including P, Mg and K. Aims: To assess the impact of their addition to flour on the sensory properties of white pita bread and postprandial glycaemia of healthy individuals. Methods: The study was conducted at the American University of Beirut (between February and October 2014). Plain, restored and fortified wheat flour, with macrominerals were used to prepare 3 types of bread: white pita bread (WP), restored white pita bread (WP-R) (premilling levels) and fortified white pita bread (WP-F) (double the premilling levels). Sensory characteristics of bread were assessed and postprandial glycaemia was determined using a single-blinded crossover design whereby participants consumed 1 of the 3 different types of pita bread in random order. Results: No significant difference (P > 0.05) between the different types of bread was detected using the triangle and acceptability tests, except for texture (P < 0.05). Macromineral enrichment of bread (WP-R and WP-F) significantly reduced postprandial glucose (P = 0.013) and triglyceride (P = 0.001) levels. Conclusions: Macromineral enrichment of refined carbohydrates may have a promising role in lowering postprandial glucose and triglycerides, and thus decrease their negative health consequences.. Keywords: sensory properties, glucose, triglyceride, white bread, macromineral enrichment Citation: El Khoury R; El Solh N; Olabi A; Toufeili I; Hlais S; Obeid O. Macromineral enrichment of white bread reduces postprandial glycaemia without altering sensory properties: a crossover study. East Mediterr Health J. 2020;16(11):1388–1395. https://doi.org/10.26719/2020.26.11.1388 Received: 16/05/18; accepted: 26/02/19 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 its turn acts as a cofactor for several enzymes involved in carbohydrate phosphorylation and oxidation, such Over the past few decades, there have gradual but signif- as protein kinases and phosphatases. K is also known icant changes in eating behaviour worldwide in light of nutritional transition from traditional diets rich in com- to affect glucose tolerance (5). Thus, low availability of plex carbohydrates to diets high in simple carbohydrates the above-mentioned macrominerals would be expected (1). These changes were associated with an increase in to delay postprandial cellular uptake of glucose, impair the prevalence of chronic diseases and accordingly, the phosphorylation, and eventually hinder carbohydrate recent dietary guidelines in the United States of America metabolism and energy production (10). These conditions (2) strongly emphasize the importance of reducing sim- would ultimately favour the onset and development of ple carbohydrates. Fibre, vitamin and mineral content of the different components of metabolic syndrome, espe- flour is drastically reduced by conventional milling and cially impaired glucose tolerance and diabetes (11). In this grain refinement processes. Macrominerals including P, same context, diminished insulin sensitivity is known to Mg and K, are reduced by about 69%, 74% and 84%, re- promote hypertriglyceridaemia (12); therefore, serum tri- spectively (3), and are known to improve postprandial glyceride (TG) levels are expected to increase in a setting glucose and insulin metabolism (4,5). P plays an essential of low mineral availability. role in carbohydrate metabolism via phosphorylation of Refined white flour has received extensive worldwide glucose to glucose-6-phosphate; an essential step for glucose clearance and trapping into cells (6). The need for P acceptance, since it is used to produce baked goods that is highest during the postprandial period, as indicated by are more palatable, softer in texture and have extended its reduced level after glucose ingestion and by the im- freshness. White pita bread is heavily consumed in provement in insulin sensitivity following its addition the Middle East and increasingly in Europe and North (7). Mg mediates glucose transport mechanisms into the America. Therefore, the objective of this work was to cell membranes through its effect on insulin signalling assess the impact of P, Mg and K enrichment on sensory via tyrosine kinase activity, phosphorylase B kinase ac- properties and postprandial glycaemia of white pita tivity and glucose transporter protein activity (8,9). K in bread.

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Methods American University of Beirut as described previously (16). The 3 samples used in different tests were assessed. Study design Ten grams of each type of white pita bread were prepared This study was conducted between February and October 2 hours prior to serving them and were stored in the re- 2014, according to the Declaration of Helsinki and all pro- frigerator (4°C). Panellists rated overall acceptability, ap- cedures involving human subjects were approved by the pearance, colour, odour, flavour and texture on a 9-point Institutional Review Board at the American University of hedonic scale (17). Panellists were instructed to rinse their Beirut (approval no. NUT0019). Written informed con- mouths before each sample. The order of the samples sent was obtained from all participants. The clinical trial within each set was randomized among the panellists in was registered with Clinical Trial.gov, NCT02598986. both tests. Wheat flour (80% extraction; Bakalian Flour Mills, Experiment 2: determination of postprandial Beirut, Lebanon) was used and 2 levels of mineral glucose and triglyceride supplementation were made. Restoration: minerals were added to white flour so that each kilogram contained 3.6 Independently from the first experiment, 11 healthy male g MgCO (G&G Vitamins, East Grinstead, UK) and 12.5 g volunteers were recruited and asked to maintain their 3 regular dietary habits and physical activity during the KH PO (Dyets, Bethlehem, PA, United State of America). 2 4 entire study course, and to avoid alcohol consumption Fortification: minerals were added to white flour to and unusual strenuous exercise 24 hours prior to each almost double the original levels, so that each kilogram of experimental session. Volunteers were aged 18–30 years white flour contained 7.2 g MgCO and 25 g KH PO . The 3 2 4 (mean 24.5 years) with body mass index between 18.5 and amounts of added P and Mg were considered safe since 29.9 kg/m2, without significant medical or chronic diseas- both were lower than the tolerable upper limits set at 4 g/ es, with no regular use of medication that affected body day and 350 mg/day for P and Mg, respectively (13). After weight, and without weight loss of ≥ 3% in the preceding supplementation, different types of white pita bread 3 months. were made and used for the different tests. A single-blinded, randomized crossover study was White pita bread making conducted. Each participant consumed 1 of the 3 different types of pita bread on each of 3 visits. The order of meals Bread samples were prepared as previously described was assigned randomly and the visits were separated by (14). Upon termination of the bread making process, a minimum washout period of 10 days. In each session, 3 samples from each type of bread [white pita bread overnight fasted participants were asked to ingest 90 g (WP), white pita bread-restored (WP-R) and white pita (containing 50 g carbohydrate) white pita bread within 10– bread-fortified (WP-F)] were analysed for their mineral 15 minutes and subsequently drink 200 ml water. Blood content by inductively coupled plasma mass spectrom- samples were collected at baseline (before ingestion) and etry (ICP-MS) using the standard method EPA 200 – 7/8 at 15, 30, 45, 60, 90 and 120 minutes after ingestion. Blood (15). P, Mg and K contents of WP-R were 84%, 200% and samples were centrifuged for 15 minutes at 4°C at 2500 g 60% higher than those of WP, respectively (Table 1). P, Mg and serum was stored in aliquots at −80°C until analysis. and K contents of WP-F were 260%, 410% and 230% higher Serum glucose, TG, and total P, Mg and K were measured than those of WP, respectively. P, Mg and K contents of using the Vitros 350 Chemistry System (Ortho-Clinical WP-F were almost double those of the WP-R. Diagnostics, Johnson & Johnson, New York, United State Experiment 1: difference and acceptability of America). Fasting serum insulin was determined using an ELISA kit (Diametra Millipore Corporation, Billerica, sensory tests MA, United State of America). Twenty-four healthy untrained male volunteers participated in a difference/discrimination test. Two triangular Statistical analysis tests were conducted to compare WP versus WP-R or Experiment 1: data related to triangular tests were ana- WP-F. Panellists were asked to indicate the odd sample lysed by checking the minimum number of correct re- in each set and to rinse their mouths before each sam- sponses using a binomial table with P = 0.05 (17). As for ple. A consumer acceptability test was conducted with the acceptability test, 2-way analysis of variance using 60 healthy randomly recruited panellists (29 women and the GLM procedure of SAS (version 9.02) was performed 31 men, mean age 22 years, range 19–29 years) from the as described previously (16). In the statistical model for

Table 1 Phosphorus, potassium and magnesium content of the different pita bread types Mineral Treatment WP (n=3) WP-R (n=3) WP-F (n=3) Phosphorus (g/kg) 3.20±0.01 5.90±0.00 11.60±0.00 Potassium (g/kg) 3.70±0.01 5.90±0.23 12.20 ±0.01 Magnesium (g/kg) 0.53±0.01 1.60±0.04 2.70±0.26 WP=white pita bread; WP-R=restored white pita bread; WP-F=fortified white pita bread. Results are expressed as the mean ± standard deviation (SD).

1389 Research article EMHJ – Vol. 26 No. 11 – 2020 acceptability, the response variable was the specific ac- rominerals were altered by food ingestion. Serum total ceptability variable. Factors in the model were the pan- P decreased following ingestion of all bread types, al- ellist and treatment (WP, WP-R and WP-F). The panel- though this failed to reach statistical significance. How- list was included as a random effect and treatment as a ever, the changes in serum total P were significant be- fixed effect. Means were separated by Tukey’s honestly tween bread types (P = 0.015), and serum P in WP-F bread significant difference test. For all data, significance was returned to baseline by the end of the session (Figure established at P < 0.05. 1A). Postprandial serum Mg levels experienced a gradual Experiment 2: The difference (Δ) in serum total P, and significant increase with time (P = 0.027), although Mg, K, TG and glucose was calculated. This represents no significant difference was detected among the dif- the value at each time point minus the value at time 0. ferent bread types (Figure 1B), despite their varied con- Repeated-measures analysis of variance was used to tent of Mg (Table 1). In contrast to Mg, postprandial K determine statistical significance with effects of bread levels decreased with time, although not significantly type, time, and bread type × time interaction. (Figure 1C), and were significantly different among bread types (P = 0.001). Results Postprandial TG and glucose responses Results of TG and glucose were also expressed as differ- Experiment 1 ences from baseline. The changes in postprandial serum Difference test and hedonic acceptability TG (Figure 2A) differed significantly among bread types In the triangular difference test, 13 correct answers out (P = 0.001), and WP-R and WP-F maintained lower lev- of the 24 responses were needed to show a significant els at all time points. Similarly, changes in postprandial difference. However, only 8 and 10 panellists responded serum glucose (Figure 2B) differed significantly among correctly for the WP versus WP-R and WP versus WP-F bread types (P < 0.013) and over time (P < 0.001). Serum tests, respectively (both P > 0.05). Therefore, the trian- glucose levels peaked at 30–45 minutes after ingestion gular tests did not detect any significant differences be- and the peaks were sooner with the enriched pita breads. tween the different types of bread. Thereafter, the enriched breads exhibited a faster decrease in serum glucose as compared to the WP bread, The consumer acceptability test (Table 2) found no starting from 45 minutes until the end of the experiment. significant differences for most acceptability attributes The magnitude of the decrease seemed to be synergisti- (overall acceptability, appearance, colour, odour and cally related to the mineral content of the bread. flavour; P > 0.05). Texture, however, was significantly more liked than that of the WP-F bread (P < 0.05), although no significant difference was detected between WP and Discussion WP-R or WP-R and WP-F bread. This study was designed to investigate the glycaemic Experiment 2 response of macronutrient-enriched pita bread, as well as its sensory properties. Our results showed that the Participants’ characteristics palatability of white pita bread was not affected by the Baseline fasting serum levels of glucose, insulin, homeo- addition of macrominerals, as indicated by the lack of dif- stasis model assessment of insulin resistance (HOMA-IR) ferences in the triangular and acceptability tests. How- (18), TG and total P, K and Mg were within the normal ever, a small difference in texture was detected between ranges (Table 3), and these were found to be similar be- WP and WP-F but not the triangular test, which is known tween the different experimental sessions for each type to be more attentive to differences. Hence, no major dif- of bread. ferences were observed when the bread was assessed in its entirety. Our findings are in line with other studies, Postprandial mineral responses in which addition of K, Ca and Mg salts as replacements Results were expressed as changes from baseline, which for NaCl did not yield any differences in appearance, tex- were the difference between the macromineral levels ture and taste of brown bread (19). Therefore, it can be at each time point minus their corresponding values at concluded that the addition of macrominerals to white baseline. Postprandial serum levels of the measured mac- wheat flour in an amount comparable to that found in

Table 2 Hedonic acceptability variables for the different pita bread types Acceptability variables Overall Appearance Colour Odour Flavour Texture acceptability WP 6.27±1.33 6.22±1.17 6.32±1.08 6.08±1.34 6.38±1.54 6.35±1.72a WP-R 6.25±1.49 6.32±1.56 6.52±1.19 6.23±1.28 5.87±1.78 5.95±1.84ab WP-F 6.07±1.33 6.28±1.21 6.40±1.39 6.12±1.53 5.85±1.62 5.42±1.71b P value 0.601 0.861 0.542 0.795 0.066 0.004 Results are expressed as mean ± standard deviation (SD). a,bMeans with different superscripts are statistically significant (P < 0.05) as analysed by paired t-test. WP = white pita bread; WP-R = restored white pita bread; WP-F = fortified white pita bread.

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Table 3 Baseline characteristics of the 11 participants including P, Mg and K. In support, P status was reported Mean SD to correlate with a favourable lipid profile, including increased high-density lipoprotein and decreased serum Age (yr) 23.7 2.4 TG levels (10,12). In agreement, we have recently found Weight (kg) 85.6 10.6 that the addition of P to a high-fat meal was able to alter Height (m) 1.80 0.04 postprandial lipidaemia by increasing apolipoprotein BMI (kg/m2) 26.2 2.4 B48 and decreasing apolipoprotein B100 (29). Besides, Mg Fasting serum glucose (mg/dl) 95.0 7.8 supplementation also improves postprandial lipidaemic Fasting serum insulin (μU/ml) 5.23 2.18 response in healthy individuals (30). HOMA-IR 1.23 0.54 Worldwide, daily consumption of wheat and wheat Fasting serum triglycerides (mg/dl) 92.5 29.4 products, mainly in the form of bread and pasta, is about 180 g per capita and this contributes to about 20% of total Fasting serum phosphate (mg/dl) 3.76 0.53 energy intake (31). Even with a consumption of 500 g/ Fasting serum potassium (mg/dl) 4.74 0.38 day of WP-R, which is considered an excessive amount Fasting serum magnesium (mg/dl) 1.95 0.21 compared to the reported daily consumption of about 150 Results are expressed as mean and standard deviation (SD). BMI = body mass index; HOMA-IR = homeostatic model assessment of insulin resistance. g per day (32) and is equivalent to around 4604.6 kJ (1100 kcal), the upper limit for both P and Mg would not be reached. The high palatability of white pita bread makes whole wheat flour, and even in double quantities, does it popular and a major contributor to overall glycaemic not significantly affect acceptability of white pita bread. load, which increases the risk of development of diabetes, The reduction in serum P following ingestion of the abnormal lipid profile and obesity (33,34). different types of bread was in line with other studies Nonetheless, the health benefits of whole wheat (7,20), and this is mediated by insulin, which is known to cereal products are reported not to be related to their fibre stimulate peripheral uptake of both glucose and P. Thus, content (35); therefore, our findings may partially explain insulin favours glucose phosphorylation (21) in a manner the benefits of whole wheat products that are known to that mimics the action of glucokinase activators (22). The have high content of macrominerals, specifically P, Mg inability of WP and WP-R to normalize serum P (return and K. Even though the beneficial effects of whole grains to baseline at 120 minutes) unlike that of WP-F (7) implies have been widely publicized, the adoption of diets rich that their P content was not sufficient to meet the needs in whole grains is still facing resistance, probably due to of intracellular phosphorylation. Moreover, the observed their low palatability. nonsynergistic relation between Mg content of the bread The major limitation of this study was that and changes in postprandial serum Mg is likely to result postprandial insulin and other appetite hormone levels from the ability of P to potentiate insulin sensitivity were not measured. In addition, the contribution of each (7,23,24), which is known to stimulate Mg clearance mineral to the observed changes was not clear. Further (20). Furthermore, improvement in insulin sensitivity studies are required to determine the postprandial may have also been attributed to the nonsynergistic response of prediabetic and diabetic patients, as well relation between K content of bread and changes in as the long-term impact of macronutrient enrichment postprandial serum K levels. Likewise, Mg (25,26) and on diabetes and different components of the metabolic K (27) are reported to improve glucose clearance and syndrome. insulin sensitivity. The ability of macrominerals (P, Mg and K) to enhance their own intracellular uptake may help to explain the reported inverse association between Conclusion P intake and blood pressure (28). This further implies White wheat flour enrichment with macrominerals (P, that postprandial levels of these macrominerals depend Mg and K) did not affect the palatability of white pita on a balance between their availability in the circulation bread, while postprandial glucose and TG levels were re- and their capacity for intracellular uptake and storage, duced. Furthermore, this supports the benefit of increas- and this implies that their circulating level is not a good ing the consumption of whole grain wheat, since it re- indicator of their bodily status. tains most of its mineral content. This study successfully At the glycaemic level, the inverse association between identified the beneficial role of minerals in improving the macromineral content of bread and postprandial the glycaemic response of a simple carbohydrate product, glucose level, especially from time 60 minutes (7), may white pita bread. The data may prove useful to ameliorate have been the outcome of an improvement in glucose the detrimental potential effect of simple carbohydrates. clearance due to the capacity of the added minerals to The work was supported by the Farouk Jaber improve glucose phosphorylation and insulin sensitivity. Funding: Furthermore, this capacity may have also contributed to Innovative Biomedical Research Award from the Faculty the observed reduction in serum TG after ingestion of of Medicine, American University of Beirut. Award num- enriched bread (WP-R and WP-F). Our findings suggest ber 100410. The funder had no role in the design, analysis that postprandial glucose and TG levels, especially or writing of this article. from 60 minutes, are dependent on exogenous factors Competing interests: None declared.

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Figure 1 Postprandial changes in phosphorus (A), magnesium (B) and potassium (C) following the ingestion of different pita breads. All values are presented as mean and standard error of the mean. The difference reflects changes between the variable at each time point and the same variable at baseline (t = 0)

0.2 A 0.1

-0.1 Two way ANOVA Bread: P = 0.015 -02 Time: P = 0.121 -0.3 GroupTime: P = 0.896

-04

∆ Total phosphorus (mg/dl) -0.5

-0.6

-0.7 0 15 30 45 60 75 90 105 120 Time (min)

0.25 B 0.2

0.15

0.1 Two way ANOVA Bread: P = 0.001 0.5 Time: P = 0.083 0 GroupTime: P = 0.589

-0.05

∆ Total magnesium (mg/dl) -0.1

-0.15 0 15 30 45 60 75 90 105 120

Time (min)

0.6 C 0.4

0.2

0 Two way ANOVA Bread: P = 0.001 Time: P = 0.257 -02 GroupTime: P = 0.726 -0.4

-0.6 ∆ Total potassium (mg/dl) -0.8

-1 0 15 30 45 60 75 90 105 120 Time (min)

white pita bread white pita bread-restored white pita bread-fortiﬁed

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Figure 2 Postprandial changes in triglycerides (A) and glucose (B) following the ingestion of different pita breads. All values are presented as mean and standard error of the mean. The difference reflects changes between the variable at each time point and the same variable at baseline (t = 0)

A 10 5

-5 Two way ANOVA Bread: P = 0.001 -10 Time: P = 0.083 GroupTime: P = 0.589 -15

∆ Total triglycerides (mg/dl) -20

-25

0 15 30 45 60 75 90 105 120

Time (min)

B 35 30

15 Two way ANOVA 10 Bread: P = 0.013 Time: P = 0.001 5 GroupTime: P = 0.388 0

∆ Total glucose (mg/dl) -5

-10

-15 0 15 30 45 60 75 90 105 120

Time (min)

white pita bread white pita bread-restored white pita bread-fortiﬁed

Enrichissement en macro-minéraux du pain blanc et réduction de la glycémie postprandiale sans altération des propriétés sensorielles : étude croisée Résumé Contexte : On sait que le métabolisme des glucides raffinés, qui sont associés à des effets nocifs sur la santé, est affecté par les macro-minéraux, notamment le phosphore, le magnésium et le potassium. Objectifs : Évaluer l’impact de l’ajout de ces macro-minéraux à la farine sur les propriétés sensorielles du pain pita blanc et sur la glycémie postprandiale d’individus en bonne santé. Méthodes : La présente étude a été menée à l’Université américaine de Beyrouth (entre février et octobre 2014). De la farine nature, de blé germé et enrichie en macro-minéraux a été utilisée pour préparer 3 types de pain : du pain pita blanc, du pain pita blanc à la farine de blé germé (degrés de prémouture) et du pain pita blanc enrichi (degrés de prémouture multipliés par deux). Les caractéristiques sensorielles du pain ont été évaluées et la glycémie postprandiale a été déterminée à l’aide d’un modèle croisé en simple aveugle, dans lequel les participants ont consommé un des trois différents types de pain pita dans un ordre aléatoire.

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Résultats : Aucune différence significative (p > 0,05) entre les différents types de pain n’a été détectée à l’aide de la méthode triangulaire et des tests d’acceptabilité, à l’exception de la texture (p < 0,05). L’enrichissement en macro-minéraux du pain (à la farine de blé germé et à la farine enrichie) a permis de réduire significativement les taux de glucose (p = 0,013) et de triglycérides (p = 0,001) postprandiaux. Conclusions : L’enrichissement en macro-minéraux des glucides raffinés peut jouer un rôle prometteur dans la diminution du glucose et des triglycérides postprandiaux, et ainsi diminuer leurs conséquences néfastes sur la santé.

إغناء اخلبز األبيض باملعادن الكبرية ُي ِّفض نسبة السكر يف الدم بعد األكل دون تغيري اخلصائص احلسية: دراسة باملناوبة رانيا اخلوري، نور ُّالصلح، عامر ُالعلبي، عامد الطفييل، ساين حليس، عمر عبيد اخلالصة اخللفية: من املعروف أن املعادن الكبرية بام فيها الفوسفور واملجنيسيوم والبوتاسيوم ّتؤثر عىل التمثيل الغذائي للكربوهيدرات ُامل ّنقاة التي ينجم عنها آثار صحية ضارة. األهداف: هدفتهذه الدراسة إىل تقييم تأثري إضافة املعادن الكبرية إىل الدقيق عىل اخلصائص احلسية للخبز العريب األبيض وسكر الدم بعد األكل لدى األفراد ّاألصحاء. طرق البحث: ُأجريت الدراسة يف اجلامعة األمريكية يف بريوت )يف الفرتة بني فرباير/شباط وأكتوبر/ترشين األول/ 2014(. ُوي َستخدم دقيق القمح العادي ُواملستعاد ُوامل َّدعم، َّاملزودباملعادن الكبرية إلعداد ثالثة أنواع من اخلبز: اخلبز العريب األبيض، واخلبز العريب األبيض ُاملستعاد )مستويات الطحن ُامل َق(، سبواخلبز العريب األبيض ُامل َّ مدع )مضاعفة مستويات الطحن ُامل َسبق(. ُوق ّي َ ت ماخلصائص احلسية للخبز ُوح ِّددت نسبة السكر يف الدم بعد األكل باستخدام تصميم تناويب ُمفرد التعمية حيث تناول املشاركون ًنوعا ًواحدامن بني أنواع اخلبز العريب الثالثة املختلفة ٍبرتتيب عشوائي. p< p> النتائج: مل ُي َكتشف ُّ أيتباين كبري )0.05 ( بني خمتلف أنواع اخلبز باستخدام اختبارات املثلث واملقبولية، باستثناء القوام )0.05 (. َّوأدى p إغناء اخلبز باملعادن الكبرية )اخلبز العريب األبيض ُاملستعاد واخلبز العريب األبيض ُامل َّ م( دعإىل انخفاض مستويات اجللوكوز بعد األكل )0.013= ( وثالثي جليسرييد الدم )p=0.001( ٍبصورة ملحوظة. االستنتاجات: قد يكون إلغناء الكربوهيدرات ُامل ّنقاة باملعادن الكبرية ٌدور ٌواعديف خفض الغلوكوز وثالثي غليسرييد الدم بعد األكل، وبالتايل احلد من آثارها السلبية عىل الصحة.

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Charlton KE, Macgregor E, Vorster NH, Levitt NS, Steyn K. Partial replacement of NaCl can be achieved with potassium, magnesium and calcium salts in brown bread. Int J Food Sci Nutr. 2007 Nov;58(7):508–21. http://dx.doi.org/10.1080/09637480701331148 PMID:17852502 20. Rosenbloom AL. Serum calcium and magnesium decline during oral glucose tolerance testing in children and adolescents with preclinical diabetes mellitus less than in normals. Metabolism. 1977 Sep;26(9):1033–9. http://dx.doi.org/10.1016/0026- 0495(77)90021-x PMID:895534 21. Amanzadeh J, Reilly RF. Hypophosphatemia: an evidence-based approach to its clinical consequences and management. Nat Clin Pract Nephrol. 2006 Mar;2(3):136–48. http://dx.doi.org/10.1038/ncpneph0124 PMID:16932412 22. Meininger GE, Scott R, Alba M, Shentu Y, Luo E, Amin H, et al. Effects of MK-0941, a novel glucokinase activator, on glycemic control in insulin-treated patients with type 2 diabetes. 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Rationing access to total hip and total knee replacement in the Islamic Republic of Iran to reduce unnecessary costs: policy brief

Mohammad Soleimani,1 Shoresh Barkhordari,1 Farhad Mardani,2 Nasrin Shaarbafchizadeh3 and Fatemeh Naghavi-Al-Hosseini4

1Faculty of Medical Science, Isfahan University of Medical Sciences, Isfahan, Islamic Republic of Iran. 2Faculty of Dental Science, Isfahan University of Medical Sciences, Isfahan, Islamic Republic of Iran. 3Health Management and Economics Research Center, Faculty of Management and Medical Infor- mation, Isfahan University of Medical Sciences, Isfahan, Islamic Republic of Iran. 4Faculty of Pharmaceutical Science, Isfahan University of Medical Sciences, Isfahan, Islamic Republic of Iran. (Correspondence to: Fatemeh Naghavi-Al-Hosseini: [email protected]).

Abstract Rationing health services is an inseparable part of the health system of any country in order to achieve universal health coverage. Elective surgery for total hip and total knee replacement places a high financial burden on health systems. Such surgery should be done in a way to ensure that the people who most need it receive the service. Models for rationing total hip and knee replacement surgery were reviewed to suggest the best policy for rationing such surgery in the Islamic Re- public of Iran. We propose a system with three main tools: clinical guidelines, gate keepers and waiting lists, with shared decision-making as an auxiliary tool. Patients should be scored at the primary health care level based on clinical and radiographic examination, alternative treatments (conservative treatments) and risk factors, with a set threshold for referral. Patients whose scores are above the threshold should be referred to secondary health care. These patients should be assessed again by specialists based on age, bone condition, surgery risk and other alternative treatments. Patients whose scores are above the threshold should be put on the waiting list for surgery. Keywords: arthroplasty, replacement, knee, hip, elective surgery, health services, policy, Iran Citation: Soleimani M; Barkhordari S; Mardani F; Shaarbafchizadeh N; Naghavi-Al-Hosseini F. Rationing access to total hip and total knee replacement in the Islamic Republic of Iran to reduce unnecessary costs: policy brief. East Mediterr Health J. 2020;26(11):1396–1402. https://doi.org/10.26719/ emhj.20.109 Received: 04/04/19; accepted: 17/10/19 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 Main problem Health costs have increased faster than global economic The fast-growing increase in osteoarthritis in low- and growth over the past 15 years (1), which is an important middle-income countries is similar to the increase in issue for health systems. Financial resources allocated high-income countries. Some studies have reported a to health services are generally inadequate, especially faster increase in some low- and middle-income coun- in developing countries . As a result these services have tries, which could be associated with low levels of educa- only a small effect on public health and tend to benefit tion in these countries (9–11). According to a study in the rich people more (2). One of the solutions to this problem Islamic Republic of Iran, the prevalence of osteoarthritis that the World Health Organization has promoted as a was 16.6% in urban areas and 20.5% in rural areas (12). prerequisite for achieving universal health coverage is Arthritis is the second leading disease causing long- rationing (3). Rationing has been referred to as not pro- term disability in individuals with the disease globally. viding services, which are considered to have benefits, to The years spent with disability from arthritis increased some people (4). by about 75% between 1990 and 2013 (13). In 2015, among Surgical operations for the total hip replacement 34 European and some Asian countries, on average and total knee replacement impose a large financial 282 total hip replacements and total knee replacements burden on the health system. Although these surgeries were done per 100 000 people (14). According to reports are mostly considered as the last-resort solution for of one of the main social insurance organizations in the treatment, studies show that nonsurgical treatments, Islamic Republic of Iran, primary orthopaedic surgery such as physical therapy, can be more effective in hip and has been an obligation of insurance organizations since knee osteoarthritis compared with having no treatment 2000. There are fewer than 10 000 knee surgeries a year (5). The increased average age of the world population in the country, but this figure is likely to reach to 30 000 and the higher prevalence of obesity and osteoarthritis in the next 5 years. The cost of this operation was high together with increased health costs have led to concerns before the 2014 health system reform plan in the Islamic about the health system’s capacity to provide these Republic of Iran, but the operation is now covered procedures and consequently the need for rationing to by insurance at a percentage rate of charge or free of ensure that people in most need have access to them charge (15). However, because of weaknesses in the plan, (1,6–8). especially an inadequate referral system, cost issues and

1396 Review EMHJ – Vol. 26 No. 11 – 2020 ineffective negotiation with insurance companies, more and knee surgery than people with normal weight (22). reforms in health system policies are needed (16). Obesity has also been associated with an increase in admission time in the hospital for people undergoing Aim of the policy brief joint surgery (23). However, such a threshold would We aimed to develop a policy brief that helps the health seem to deprive many people who are highly in need system in the Islamic Republic of Iran to ration elective of this surgery of receiving it (24). Usually, total knee hip and knee joint replacement surgery in an equitable replacement is not done in people younger than 50 years and clinically beneficial way. or older than 80 years (25). In younger people, this is because of the potential complications of the surgery, and in older people this is because of their muscular condition Methods and lack of movement and exercise, which can reduce the We developed this policy brief through a literature effectiveness of these operations (26). review and group discussions among ourselves. We searched PubMed, Scopus, Web of Science, Embase, and Gate-keeper system Google Scholar up to 2019 using the keywords in English: In a gate-keeper system, people cannot access second-lev- “rationing”, “hip replacement”, “knee replacement” and el services such as the hospital and specialist physician “elective surgery”. In addition, the Guideline of American without referral by a general practitioner. This system College of Rheumatology on hip and knee osteoarthritis has two main benefits: (i) cost control by reducing unnec- (17) and the clinical guidelines of the Iranian Orthopaedic essary interventions, and (ii) use of effective secondary Society were used to assess the use of guidelines. services because physicians are better informed than patients about the quality of services provided by secondary Policy options providers (27). Different tools have been used in rationing. These tools A study showed that 97% of people with severe knee include waiting lists, clinical guidelines and gate-keeper problems, who were receiving secondary services, had systems. Shared decision-making is an auxiliary tool that initially seen a general practitioner (28). Another study has been effective in cost reduction but it has not been showed that only 67% of orthopaedic referrals by general used as a tool on its own. In most countries, these tools practitioners were appropriate (29). For appropriate have been used together, but to facilitate our analysis, we referral, we need a referral threshold based on a clinical evaluated the tools separately. guideline that is available to general practitioners, such systems have been used in different countries. A Clinical guidelines review study proposed that general practitioners should Clinical guidelines are used in New Zealand and the Unit- consider four factors in referral for joint surgery: (i) Do ed Kingdom of Great Britain and Northern Ireland at the clinical and radiographic characteristics of the patient micro-level where rationing is based on the views of phy- justify the referral?; (ii) Has the patient had appropriate sicians of indications and contraindications for a medi- conservative treatments?; (iii) Does the patient have cal service (18). However, in developing countries, this risk factors that might adversely affect the outcome of method is used at a higher (meso-) level where insurance surgery?; and (iv) Can these risk factors be modified? (20) providers and hospitals determine the clinical guidelines. In a study in Switzerland in 2000, 20% cost reduction The main feature of the use of clinical guidelines is the was observed as a result of the gate-keeper system (30). use of evidenced-based medicine. However, there are many disagreements on the indications and contraindi- Waiting lists cations for total knee replacement surgery (19). Two methods have been used to include the people on a In the studies we reviewed, rationing using clinical waiting list. In the queue-based model, people are includ- guidelines is not only considered an independent method ed on the waiting list based on the time of their referral, of rationing but also an integral part of implementation regardless of disease severity. This method is a chance- of other rationing methods. For example, the American based prioritization. The other model is a scoring model College of Rheumatology proposes conservative where an individual’s position on the waiting list is based treatments such as water therapy and aerobic exercise on specific scores for severity and need (6). for patients with osteoarthritis rather than surgery (17). Different scoring systems are used in different The clinical criteria of age, bone status, surgical risk, countries to accommodate individuals on the waiting preoperative procedures and motor limitations have list for joint replacement surgery. The most commonly been used to determine whether surgery is appropriate used systems are the Oxford hip and knee score, reduced for patients with osteoarthritis or not (20). Western Ontario McMaster osteoarthritis index In 2006, the United Kingdom established a threshold (WOMAC) score, New Zealand Orthopaedic Association of body mass index less than 30 kg/m2 for knee and hip score, clinical priority assessment criteria, and the score surgeries. As a result, 8452 pelvic surgeries and 12 929 of the multi-attribute arthritis prioritization tool (6,31–33). knee surgeries were eliminated, with a significant cost According to the New Zealand Orthopaedic reduction (21). Obese people were 1.3 times more likely Association system, patients are scored from 0 to 100. to have postoperative complications from shoulder, hip After referral, each patient is scored by a consultant and

1397 Review EMHJ – Vol. 26 No. 11 – 2020 a nurse at the first visit with the specialist. Based on a Clinical guidelines are necessary for rationing, and defined threshold limit appropriate for conditions in the countries should develop guidelines relevant to their country, patients below the threshold are referred back to context. The Iranian Orthopaedic Association published the general practitioner. Patients above the threshold limit a clinical guideline on joint replacement surgery in 2016. are referred to the orthopaedic department and evaluated However, this guideline has not yet been implemented, by a surgeon, who manages the waiting list. A study in so no cost–effectiveness assessment could be done (39). New Zealand indicated that of 608 patients examined, 32% were referred back to the general practitioner based Waiting list on this threshold, thus reducing the number of patients Although a scoring-based waiting list is preferred to a list on the waiting list (33). based on the time entered on the list, both methods have In England, the use of the Oxford hip and knee score reduced costs. It should be noted that more developed for knee surgery resulted in a cost reduction of £11.8 countries have moved from a queuing model to a scoring million a year (£ 1 = US$ 1.6041 in 2011, the date of the model. cited study) (31). The Oxford hip score questionnaire was Gate-keeper system translated into Farsi for use in the Islamic Republic of Iran for pre-operative total hip replacement patients (34). As shown in Figure 1, gate keepers are the first line of ra- The adapted and validated Iranian version of the Oxford tioning. Since most people with serious joint problems go hip score questionnaire was found to be reliable and to general practitioners first and the referrals of general practicable for use with Iranian patients (34). practitioners have been effective for accessing treatment (40), this rationing tool is recommended. In addition, Shared decision-making an appropriate referral threshold can make the refer- Clinical shared decision-making is not discussed as means rals more effective. Given the unsuccessful experience with an urban referral system in the Islamic Republic of of rationing, but can be considered an auxiliary tool for Iran in 2005, a system should be designed with a refer- rationing. Shared decision-making can contribute to fair ral threshold based on clinical guidelines. This system rationing along with other tools. Research has shown should be piloted and the results evaluated. that patients are willing to share in the decision-making for their health care (6). In the United Kingdom, it was Proposed rationing system shown that individuals consider pain severity, inability We propose a system summarized in Figure 1 with three to walk, costs and postoperative care some of the clinical main tools: clinical guidelines, gate keepers and waiting criteria for joint replacement surgery (20) . Another study lists, with shared decision-making as an auxiliary tool. showed that 44–55% of people who required total knee For patients to enter the rationing system for treatment replacement and total hip replacement were certainly or through the gate keeper, they must be scored first by the probably unwilling to have surgery (35). In another study, primary health care units based on clinical and radio- if individuals were consulted about their willingness to graphic examination, alternative treatments (conserv- have surgery after the complications and conditions of ative treatments) and risk factors. Patient whose scores the surgery were explained, a 36% cost reduction in joint are below the threshold, should be referred by general replacement surgery was seen (36). Thus, prioritization of practitioners to physiotherapists for conservative treat- patients on the waiting list can be based on clinical cri- ment such as hydrotherapy and exercise. Patients whose teria and the views of the patients themselves about the scores are above the threshold, should be referred to need for surgery (37). secondary health care units. At this stage, patients are Policy recommendations assessed by specialists and are scored on age, bone condition, risk of surgery and other alternative treatments. Based on our evaluation of the various methods for ra- Patients whose scores are below this threshold will be re- tioning surgical care (clinical guidelines, waiting lists, ferred to physiotherapists again. Patients whose scores gate-keeper systems, and shared decision-making), are above the threshold should be placed on a waiting list Table 1 lists the disadvantages, benefits, and policy op- and prioritized according to age, sex, body mass index, tions for each method. occupation and history of total knee or hip replacement. Clinical guidelines As illustrated in Figure 1, decision-making should be actively shared with patients; they should be encouraged to Clinical guidelines are the basis of the rationing method share their ideas about treatment and other options that in many cases. Most clinical guidelines are based on ev- may be available. idence; however, clinical guidelines can also be based on consensus (38). Implementation of recommendations The policy implemented in the United Kingdom In order to implement the recommendations in our pol- to establish a threshold linked to body mass index is icy brief at the mid-level in the Islamic Republic of Iran, a special type of rationing based on clinical guidelines. the following process should be followed. First, establish Although this policy had many critics, it did reduce costs a policy-makers’ group consisting of heads of universities and time to admission to hospital (16) . Furthermore, of medical sciences, heads of hospitals, representative of the age of people can determine candidates for surgery. the orthopaedic association, insurance providers, trusted

1398 Review EMHJ – Vol. 26 No. 11 – 2020 Implementation level Iranian Orthopaedic Association Insurance providers Universities of medical sciences Hospitals Iranian Orthopaedic Association Insurance providers Hospitals Universities of medical sciences Iranian Orthopaedic Association Insurance providers Universities of medical sciences Iranian Orthopaedic Association Insurance providers • • • • • • • • • • • • •

Policy option Age Bone state Surgical threshold considering the following factors, among others: Review and modify the national local clinical guidelines Prioritize based on the clinical guideline Clarify prioritization processes using television advertisements and posters in hospitals Demand reduction Use the private sector for to get operations sooner (for people who don’t want to be on a waiting list) Formulate referral thresholds based on clinical guidelines considering the following items: Identify failure factors of the Iranian urban referral system project Clarify prioritization processes and define thresholds in the presence of patient or his/her representative Clarify surgical processes and postoperative complications with the patient • • • • • • • Clinical features and radiography Conservative measures (water therapy and aerobic exercise) Risk factors • • • Disadvantages Disagreements on existing indications Lack of attention to specific preferential treatments for patients Failure to remove some indications due lack of proof ineffectiveness Failure to use and assess the national clinical guidelines Negative effect on Fairness Lack of a valid index to make prioritization on the list model Prolonged waiting time Negative effects of prolonged waiting time Need for legislative and motivational infrastructure for implementation Despite increased quality of referrals with clinical guideline, number of referrals does not change Unsuccessful experience of implementing urban referral system in the Islamic Republic of Iran Need to formulate a referral threshold based on the clinical guidelines Inability of patient to understand clinical decisions Need for a separate appointment with the physician • • • • • • • • • • • • • • Advantages Significant cost reduction in the short and long term Local clinical guideline Significant cost reduction Decreased waiting times in the short term Better quality of referrals Elimination of unnecessary services and unnecessary visits to specialists Increased use of conservative measures for those not in need of surgery Effective cost reduction No need for new infrastructure Greater trust in prioritization • • • • • • • • • • Advantages and disadvantages of methods for rationing Tool Clinical guideline Waiting list Gate-keeper system Shared decision-making Table 1

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Figure 1 Optimized policy recommendations for rationing total hip replacement (THR) and total knee replacement (TKR) surgery

Pathway for patient requiring THR and TKR

Shared decision making

Secondary health care (Specialist) Primary health care unit (general practitioners) Patient Put on a waiting REFER assessment list based on: Upper • Age Patient for THR or TKR Upper threshold Surgery threshold • Gender assessment for Referral threshold threshold • BMI referring to the Lower treshold • job status specialist • History of THR and TKR Conservative lower threshold treatment

orthopaedic surgeons, representative of general practi- surgery based on the clinical guidelines. Fourth, reach an tioners and physiotherapists. Establish a research group, agreement with insurance providers and patient repre- consisting of for example general practitioners, special- sentatives on the cost of treatment that insurance covers. ists and statisticians, to evaluate and validate the clinical Funding: National Agency for Strategic Research in guidelines developed in 2016 by the Iranian Orthopaedic Medical Education, Tehran (grant no. 971935). Association. Second, modify the clinical guidelines based on the results. Third, establish thresholds for referral and Competing interests: None declared.

Limitation des interventions de prothèse totale de la hanche et du genou en République islamique d’Iran en vue de réduire les coûts inutiles : note d’orientation Résumé La limitation des services de santé est une composante indissociable du système de santé de tout pays dans l’objectif de parvenir à la couverture sanitaire universelle. La chirurgie programmée pour la prothèse totale de la hanche et du genou constitue une lourde charge financière pour les systèmes de santé. Cette chirurgie doit être effectuée de manière à ce que les personnes qui en ont le plus besoin en bénéficient. Les modèles de limitation de la chirurgie totale de la hanche et du genou ont été examinés afin de proposer la meilleure politique pour limiter ce type d’intervention en République islamique d’Iran. Nous proposons un système comportant trois outils principaux : les lignes directrices cliniques, les filtres et les listes d’attente, avec la prise de décision partagée comme outil auxiliaire. Les patients doivent être évalués au niveau des soins de santé primaires sur la base de l’examen clinique et radiographique, des traitements alternatifs (traitements conservateurs) et des facteurs de risque, avec un seuil défini pour l’orientation-recours. Les patients dont les scores sont supérieurs au seuil doivent être orientés vers les soins de santé secondaires. Ces patients doivent être réévalués par des spécialistes en fonction de leur âge, de leur condition osseuse, du risque chirurgical et d’autres traitements alternatifs. Les patients dont les scores sont supérieurs au seuil doivent être ensuite placés sur la liste d’attente des interventions chirurgicales.

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ترشيد عمليات االستبدال ُالك ِّل َللو ْرك واالستبدال ُالك ِّ لللركبة يف مجهورية إيران اإلسالمية لتقليل التكاليف غري الرضورية: موجز السياسات حممد سليامين، شورش برخورداری، فرهاد مرداين، نرسین شعربافچی زاده، فاطمه نقوی احلسینی اخلالصة ُيعد ترشيد اخلدمات الصحية ً جزءاال يتجزأ من النظام الصحي يف أي بلد من أجل حتقيق التغطية الصحية الشاملة. ُوت ِّثل اجلراحة االختيارية لالستبدال ُالك ِّل َللو ْرك واالستبدال ُالك ِّل للركبة ًعبئا مالي ً ا ً كبرياعىل ُّالنظم الصحية. وينبغي إجراء هذه اجلراحة عىل ٍنحو يضمن حصول األشخاص الذين هم يف َأم ِّ ساحلاجة إليها عىل اخلدمة. ُواست ِعرضت نامذج ترشيد جراحات االستبدال ُالك ِّ لللورك واالستبدال ُالك ِّل للركبة القرتاح أفضل سياسة لرتشيد مثل هذه اجلراحات يف مجهورية إيران اإلسالمية. ونقرتح ًنظاما يشتمل عىل ثالث أدوات رئيسية: املبادئ التوجيهية الرسيرية، ومراقبو البوابات، وقوائم االنتظار، مع عملية اختاذ قرار مشرتكة كأداة مساعدة. وينبغي إعطاء درجات للمرىض عىل مستوى الرعاية الصحية َّاألولية ًبناء عىل الفحص الرسيري والتصويري، والعالجات البديلة )العالجات التحفظية(، وعوامل اخلطر، مع حتديد ٍّحد أدنى لإلحالة. وينبغي إحالة املرىض الذين تتجاوز درجاهتم َّاحلد األدنى إىل الرعاية الصحية الثانوية. وجيب تقييم هؤالء املرىض ًمرة أخرى من ِبلق املتخصصني عىل أساس العمر وحالة العظام واملخاطر اجلراح ةي والعالجات البديلة األخرى. وينبغي وضع املرىض الذين تتجاوز درجاهتم احلد األدنى عىل قائمة االنتظار للخضوع للجراحة.

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Application of geographic information systems in maternal health: a scoping review

Leila Ahmadian,1 Fatemeh Salehi2 and Kambiz Bahaadinbeigy3

1Medical Informatics Research Centre, Institute for Futures Studies in Health, Kerman University of Medical Sciences, Kerman, Islamic Republic of Iran. 2Health Human Resources Research Centre, School of Management and Information Sciences, Shiraz University of Medical Sciences, Shiraz, Islamic Republic of Iran. 3Gastroenterology and Hepatology Research Centre, Institute of Basic and Clinical Physiology Sciences, Kerman University of Medical Sciences, Kerman, Islamic Republic of Iran. (Correspondence to: Fatemeh Salehi: [email protected]).

Abstract Background: Improving maternal health is a global health priority and requires accurate evaluation of factors affecting maternal health. Geographic information systems have been used to explore maternal health problems. Aims: The aim of this study was to identify studies that used geographic information systems in the field of maternal health care and to determine maternal health and mortality variables visualized on these systems. Methods: This was a scoping review in which we systematically searched PubMed and Science Direct for studies that used geographic information systems to evaluate maternal health care. We included all relevant cross-sectional studies published in English between December 1995 and December 2017. We extracted the following information from each study included: study year, region, objectives, type of geographic information system used, variables visualized by the geographic information system, and all other variables examined that related to maternal health. Results: Of 5240 articles initially retrieved, 40 were included for detailed review. Most of the studies (n = 32) were done in developing countries in Africa, Asia, and Latin America and the Caribbean. Most of the studies (n = 33) visualized mothers’ distance to health facilities and travel time to health care centres on geographic information systems. Other factors examined included antenatal care capacity (n = 4) and capacity of maternal health services (n = 3). Conclusions: Comprehensive research on the application of geographic information systems in maternal care is lacking. Most studies applied simple descriptive mapping of spatial distribution patterns with a few relevant variables. Keywords: geographic information system; maternal health; maternal health services; health services research Citation: Ahmadian L; Salehi F; Bahaadinbeigy K. Application of geographic information systems in maternal health: a scoping review. East Mediterr Health J. 2020;26(11):1403–1414. https://doi.org/10.26719/emhj.20.095 Received: 28/06/18; accepted: 26/09/19 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 helped health experts to improve health care. These improvements have helped health care professionals Maternal health is a globally important health challenge. work more efficiently and effectively (5,6). Recently, Maternal health refers to the health of women during researchers have started to apply geographic information pregnancy, childbirth and the postpartum period (1). Ac- systems (GIS) to explore maternal and newborn health cording to the World Health Organization (WHO) the problems (7–9). GIS help to show regional variations and global maternal mortality rate is unacceptably high and about 810 maternal deaths occur daily around the world abnormal patterns of health characteristics. Through with 94% of all maternal deaths occurring in developing the use of GIS, researchers can gain insight into the countries (2). In 2015, 295 000 women died following use of health services and expose health problems and pregnancy related complications – most of these deaths environmental risks. This technology can be easily used were in low-resource settings and most could have by non-geographers with basic computer literacy and been prevented (2).The Sustainable Development Goals map-reading skills (10). The use of GIS is a means to (SDGs) now call for an acceleration in progress in order effectively link and analyse the range of data necessary to achieve a global maternal mortality rate of 70 mater- to address complex questions in health promotion, public nal deaths per 100 000 live births, or less, by 2030 (3). health, community medicine, epidemiology, and other Achieving this global goal will require countries to reduce fields (11). their maternal mortality rate by at least 7.5% each year Despite a number of reviews on the use of GIS in between 2016 and 2030 (3). Reducing maternal mortality maternal health (12–16), to the best of our knowledge, no was introduced globally as an important health priority review has collectively analysed the results of studies in the United Nations Millennium Development Goals to determine maternal health and mortality factors (4). Precise evaluation of the maternal mortality rate is visualized through GIS. Some studies have shown the first step to reducing this rate. that the application of GIS in maternal health can help Extensive implementation of various software and decision-making on policies to reduce maternal problems information technology services in recent years has and improve maternal care outcomes (17,18). Therefore,

1403 Review EMHJ – Vol. 26 No. 11 – 2020 we did a scoping review to identify GIS studies related to review studies, editorials, commentaries and letters; maternal health care to determine maternal health and studies that had not visualized data on GIS; and articles mortality factors (variables) visualized through GIS. We not in English. also summarized other variables investigated, but not visualized through GIS, to get a general overview of all Review strategy evaluated variables in the included studies. The results Two reviewers independently screened and assessed the of our review can be used to help in planning to reduce titles and abstracts of the retrieved articles. The review- preventable causes of maternal health problems. Our ers met and reached consensus at the end of the screen- results can also help determine gaps in the use of these ing process. In cases of disagreement, a third independ- types of data and provide a road map to guide more ent reviewer was consulted to resolve the disagreement. precise studies on various aspects of maternal health. We compared the results of the independent screenings using the kappa statistic (kappa = 8.6). The reviewers Methods were blinded to each other’s decisions to control for assessment bias. We also checked the reference lists of the Search terms articles retrieved for other relevant studies. We devel- We searched for relevant articles in English from 1995 oped a data collection form and extracted the following to 2017 using PubMed and Science Direct databases. information from each paper: study year, region, objec- We used two groups of key search terms. Group A in- tives, GIS application type, variables visualized by GIS, cluded GIS-related terms: GIS; geographic information and all other variables examined that related to maternal system; risk mapping; spatial analysis; spatial data; GPS; health. We examined the extraction forms for coverage, and health mapping. Group B included terms related to clarity and content validity in several meetings. We di- maternal health: maternal mortality; maternal health; vided the extracted variables from the studies into two maternal care; pregnancy; delivery; and maternal death. groups: subvariables and variables directly visualized on Our search strategy was as follows: first we used “OR” to GIS. Based on expert consensuses and in order to better combine the terms within each group A and B separately. report on the variables, we classified the subvariables Then, we combined keywords from the two groups using into six categories: (1) maternal factors, (2) socioeconomic the “AND” operator to find all the studies that used GIS in factors, (3) health care service factors, (4) ecological deter- the field of maternal care. We then limited the search in minant factors, (5) environmental factors, and (6) health both databases to humans and studies published in Eng- related factors. lish. Results Inclusion and exclusion criteria The inclusion criteria were: cross-sectional study relat- Study selection ed to the use of GIS in maternal health care; published In our initial search of the online databases we found between December 1995 and December 2017; in English; 5240 articles (Figure 1). After our first screening of titles and on a human population. The exclusion criteria were: and abstracts based on out inclusion and exclusion crite-

Figure 1 Flow diagram of the selection of papers

5240 studies retrieved: 4775 (91%) PubMed 465 (9%) Science Direct

1737 (33.1%) excluded because not 1737 (33.1%) excluded because not on humans and not in English on humans and not in English

3469 (66.2%) articles retained for title and abstract review 3268 (62.4%) excluded because did not meet the inclusion criteria 201 (3.8%) articles selected for full text review 161 (3.1%) excluded because did not meet inclusion criteria 40 (0.07%) articles included for final review

1404 Review EMHJ – Vol. 26 No. 11 – 2020 ria, we retained 201 eligible articles for further full-text six did not state which software was used to analyse the review. Based on this review of full texts, we excluded 161 data (27,33,40,47,52,57). articles as they did not meet the inclusion criteria, and Variables extracted from the studies are shown in retained 40 articles for detailed analysis. Table 2. Many studies visualized the variables: distance to health facilities (n = 16) and travel time to health care Included studies centres (n = 17). Other frequently mapped variables were Of the 40 articles we retained, all were journal papers. spatial distribution of health services and emergency Table 1 gives a description of the 40 studies – publica- obstetric care (n = 11). Socioeconomic and sociocultural tion year, objectives, region and data sources. The oldest variables, such as women’s educational level (n = 10) and articles were published in 2004 (57,58). The number of household wealth (n = 9), were often investigated. studies investigating the application of GIS for maternal care has increased since 2010. Most of the studies Discussion (n = 29) were conducted in developing countries in Afri- ca, Asia, and Latin America and the Caribbean (19–23,26– The findings of our study show that special attention has 31,33,34,36,37,39–43,45–50,53,55,58) and 11 were conducted been paid to geographic access and travel time to health in developed countries in Europe, North America, Aus- services in published literature on maternal health. Oth- tralia, New Zealand, and Japan (24,25,32,35,38,44,51,52,5 er important reported variables included: maternal age, 4,56,57). Nearly half of the studies (n = 16) were done in maternal educational level, household wealth, residential Africa because of its high maternal and infant mortality area, distribution of health services, and availability of rates (21,23,26,28,31,36,39–42,46–50,58), nine were done in emergency obstetric care facilities per population. Asia (19,20,22,27,34,37,43,53,55), 11 in the Americas and the Determining the distribution of human resources Caribbean (24,25,29,30,32,33,44,45,51,52,54), three in Europe (obstetricians/gynaecologists, maternity nurses and (35,57,56) and one in Oceania (38). midwives) can show imbalances in the distribution of health personnel. The findings of some research Each study presented data on one country/region, has shown that the educational level of women was except one study which provided data on four countries strongly correlated with the maternal mortality rate (27). Multiple data resources were used to conduct (59–63). The results of our study also showed that the studies. The source of data in 15 of the studies was mothers’ educational level was frequently reported in national statistics and censuses (Table 1). Other sources the included studies. Educational level has a positive of data included, among others, results of other previous influence on autonomy, awareness of health services, the surveys (n = 11), interviews with women and health staff health-seeking behaviour, responsibility and knowledge (n = 5) health registries (n = 6). of self-care and healthy lifestyles (64) and can directly Geographic access to health services was the most and indirectly contribute to a reduction in maternal common factor examined (n = 22) in the included studies mortality. Some believe that education may have a more (20,22,25,26,28,30,35,37,39,40,41,43,44–47,49,51,52,56–58). important role compared to economic indicators, such Other common factors examined included antenatal as income, clean water supply and sanitary sewer access care capacity (19,25,42,55) and capacity of maternal health (65). Maternal age was examined as the underlying services (21,48,53). variable in many of the studies we reviewed, and is a Most studies (n = 28) used the spatial analysis of the key variable because older women are at a higher risk of GIS software such as network analysis, buffer, hot spots death and complications during pregnancy or delivery and Moran techniques (19,22,23,26–29,31–35,37–45,48– (66,67). The risk of pregnancy-related death for mothers 50,52,53,55,56). Other studies (n = 10) used spatial mapping over 40 years between 1998 and 2005 has been reported (20,21,24,25,30,36,51,54,57,58) and two used spatial modelling to be six times higher compared with teenagers (68,69). Others research has found that young adolescents (< 15 techniques (46,47). years old) face a higher risk of complications and death Many of the studies that used GIS in maternal as a result of pregnancy (70,71). The residential area of health focused on potential geographic access to care on pregnant woman is also an important factor. Higher the basis of the spatial distribution of health facilities maternal mortality rates have been reported in women (27,35–37,44,46,47,51,52,56). Some investigated the effect living in rural areas and poorer communities (2). The of geographic access on mortality and care utilization fact that most of the studies included in our review (24,33,49,55). Other studies modelled the availability of and were conducted in developing countries, especially in access to emergency obstetric care (22,28,43,50). Africa, is understandable as, according to WHO, 94% The geospatial unit of analysis in 16 studies was of all maternal deaths occur in developing countries (2) the national level (27,28,29,31,35,36,39,40,44,46,48– and factors that threaten the health of mothers are more 50,52,56,58). Most of the studies (n = 24) used ArcGIS common in these countries. (Esri, Redlands, California, United States of America) Some research has provided evidence that comorbid (19–21,24,25,27,31,32,34,36–39,42–47,50,51,53–55) to analyse conditions such as high blood pressure, diabetes and the data, 10 studies used other types of GIS software cardiac diseases contribute to maternal deaths (72). – ArcView, QGIS, ArcInfo – (22,26,28–30,35,41,49,56,58), and Others showed that direct pregnancy complications are

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Table 1 Description of the included studies Author Publication Objectives of the study Countrya Data sources year Ansariade and Manderson, (19) 2015 Determine the influence of urban and Indonesia, Structured interview with women rural settings on antenatal care and Sulawesi who delivered birthing decisions and investigate if women’s decision on antenatal care and birth assistance are geographically clustered Jain, et al. (20) 2015 Assess the influence of economic and Pakistan Health facilities; and household geographic access to health facilities surveys on institutional deliveries Tabatabai, et al. (21) 2014 Map and analyse the capacities of United Republic Hospital questionnaire; population public and private hospitals to provide of Tanzania, census dataset maternal health care Ruvuma Sabde, et al. (22) 2014 Identify potential areas for further India, Madhya Interviews with parturient women interventions to increase the Pradesh effectiveness of the emergency obstetric transport system Mwaliko, et al. (23) 2014 Determine the association between Kenya, western Database of Webuye health and the place of delivery and the distance demographic surveillance system; of a household from the nearest health structured interviews with trained facility, and assess the demographic field assistants characteristics of households with a delivery within a demographic surveillance system Detres, et al. (24) 2014 Examine how GIS maps can be used USA, Florida Florida vital statistics birth and by local organizations to engage infant death records the community in the discussion of maternal and child health data to modify service delivery Brown, et al. (25) 2014 Determine maternal ground transport USA US census tract data; American times from community hospitals to the hospital association annual survey nearest hospital offering comprehensive (level III) neonatal care Nesbitt, et al. (26) 2014 Compare methods to measure potential Ghana Kintampo Health Research Centre spatial access to delivery care in low- surveillance data; health facility and middle-income countries assessment; Ghana registered midwives association Tatem, et al. (27) 2014 Present methods to estimate women of Afghanistan Household survey data; United childbearing age, and pregnancies and Bangladesh, Nations statistics; new estimates live births in relation to current health Ethiopia, United of stillbirths, miscarriages and infrastructure Republic of abortions from the Guttmacher Tanzania Institute McKinnon, et al. (28) 2014 Assess the effect of distance to Ethiopia Ethiopian Demographic and emergency obstetric and newborn care Health Survey; Ethiopian national services on early neonatal mortality emergency obstetric and newborn and examine whether proximity to care needs assessment (Ethiopian services contributes to socioeconomic Ministry of Health); questionnaire inequalities in early neonatal mortality filled by women Wang, et al. (29) 2014 Estimate the influence of service Haiti Haiti Demographic and Health readiness at health facilities on women’s Survey; Haiti service provision use of facility delivery care for delivery assessment survey Gaspar, et al. (30) 2014 Evaluate the spatial distribution of Brazil, Belo A system of obstetric information public sector obstetric care Horizonte Municipal (SISMater®), Department of Health of Belo Horizonte (SMSA-BH);, cohort of 2956 newborns Benedict, et al. (31) 2014 Explore geographical patterns in the Ghana Ghana Demographic and Health risk of not utilizing using a skilled birth Survey; interviews with women attendant during childbirth in women of different socioeconomic backgrounds Blake, et al. (32) 2014 Explore the geographic relationships USA, California Zip codes, US census among between dairy farms, nitrate levels in drinking water, low birth weight and socioeconomic data at the Zip code level

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Table 1 Description of the included studies (Continued) Author Publication Objectives of the study Countrya Data sources year Almeida, et al. (33) 2014 Identify spatial patterns of in Brazil, São Paulo Department of information distribution of overall, early, and late systems and information neonatal mortality rates technology of the Brazilian national healthcare system Arslan, et al. (34) 2013 Determine the spatial patterns of Turkey, Kocaeli Registry of births and deaths perinatal mortality, examine whether regional differences exist and whether these differences are linked to regional risk factors Engjom, et al. (35) 2013 Assess the availability of obstetric Norway Census data; Statistics Norway; institutions, the risk of unplanned medical birth registry delivery outside an institution and maternal morbidity in a national setting in which the number of institutions declined from 95 to 51 during over 30 years Sudhof, et al. (36) 2013 Identify potential gaps in access to Rwanda, Birth registries at in eight health emergency obstetric care Kayonza centres and the district hospital Song, et al. (37) 2013 Assess spatial accessibility to maternity China, Shenzhen Website of Shenzhen Health and units Population and Family Planning Commission Chong, et al. (38) 2013 Assess the usefulness of geospatial Australia, New New South Wales health ministry methods in identifying communities at South Wales high risk of smoking during pregnancy and timing of the first antenatal visit Bowie C, et al. (39) 2013 Evaluate geographical access to health Malawi Malawi census; Ministry of Health care facilities facility surveys Masters, et al. (40) 2013 Estimate travel times between Ghana Ghanaian Ministry of Health populations and health facilities using geospatial techniques Yao, et al. (41) 2013 Present a geographical perspective on Mozambique, Population survey data access to sexual and reproductive health Gaza province care for rural women O’Meara, et al. (42) 2013 Assess spatial autocorrelation in uptake Kenya, western Survey data of antenatal care and relationship to individual, household and village-level factors Monyet al. (43) 2013 Investigate the availability and India, Karnataka Combination of self-reporting, distribution of emergency obstetric care record review and direct services in eight northern districts of observation Karnataka State in south India Brown, et al.(44) 2012 Determine the percentage of women of USA US census tract data reproductive age living within a 30- and 60- minute drive time of the nearest tertiary care perinatal centre Friedman, et al. (45) 2012 Evaluate the effect of an inverse Haiti, central Retrospective review of operative relationship between health care district logbooks; Haiti earthquake data use and distance to care related to portal emergency and essential surgical care Gething, et al. (46) 2012 Develop a uniquely detailed set of Ghana Ghana Ministry of Health; spatially-linked data and a calibrated University of Ghana; project by geospatial model to undertake a the Ghana Ministry of Health national audit of geographical access to and Ghana Health Service Core; maternity care at birth Welfare Indicator Questionnaire survey Blanford, et al. (47) 2012 Analyse the physical access of Niger FAO Geo Network Portal; Niger populations to health facilities with Ministry of Health an emphasis on the effect of seasonal conditions and the implications of these conditions for availability of adequate health services, and provision of drugs and vaccinations

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Table 1 Description of the included studies (Concluded) Author Publication Objectives of the study Countrya Data sources year Massey, et al. (48) 2011 Identify priority regions for the Senegal National agency for demography expansion of human resources for and statistics; WHO health Gabrysch, et al. (49) 2011 Quantify the effects of distance to care Zambia National household data from the and level of care on women’s use of Zambian Demographic and Health health facilities for delivery Survey; national facility data from the Zambian health facility census Bailey, et al. (50) 2011 Provide a set of multicriteria decision Ethiopia Ethiopian national survey on analyses to help health planners make baseline assessment of emergency informed decisions about interventions obstetric and newborn care; spatial to increase access to emergency services population data from Land Scan™ population data Gjesfjeld & Jung. (51) 2011 Examine maternity care access for USA, Dakota North Dakota department of vital expectant mothers records Grzybowski, et al. (52) 2011 Systematically document newborn and Canada, British British Columbia Perinatal Health maternal outcomes in terms of travel Columbia Program distance to access the nearest maternity services with caesarean section capability Fisher and Myers (53) 2011 Test the appropriateness of new, Indonesia, Nusa Cybertracker; health data collected inexpensive and simple GIS tools in Tenggara Timur by district and subdistrict health poorly resourced areas of a developing officer departments and clinics country Bloch, et al. (54) 2011 Examine spatial patterns of USA, Census data; de-identified neighbourhood contextual factors of Philadelphia geocoded Philadelphia birth stress with preterm birth and country of records; publicly available birth (USA or elsewhere) Philadelphia police department crime statistics. Målqvist, et al. (55) 2010 Examine the association between Viet Nam, Interviews with mothers and staff; distance from the mother’s home to Quang Ninh medical records; VidaGIS database the closest health facility and neonatal mortality, and investigating investigate the influence of distance on patterns of perinatal health care use Pilkington, et al. (56) 2008 Describe the effect of maternity unit France French national perinatal surveys; closures on distance and mean travel vital statistics registries time between pregnant women’s homes and maternity units Dummer, et al. (57) 2004 Investigate whether geographical England, Cumbrian births database accessibility to hospitals affected the Cumbria risk of infant mortality Heard, et al. (58) 2004 Identify whether access to reproductive Malawi Malawi health facilities inventory; health services partly explains the use of Malawi demographic and health modern contraception survey WHO=World Health Organization; GIS=geographical information system; USA=United States of America; FAO=Food and Agriculture Organization. aWhere the region is not specified, the study done at the national level. the leading causes of maternal deaths (73). Little attention and maternal and perinatal mortality (34,74). Although we was paid to these health factors in the studies in our believe there is a relation between the above-mentioned review, which may be because the data sources used in groups of variables and maternal mortality, it is difficult these studies did not include these kind of health-related to know which variable is the strongest determinant. In factors. addition, the strength of the association of these variables with maternal mortality may differ by region. However, The articles included in our study used and combined proposing a dataset for research in this field would direct various data sources, which provides better results and researchers to a unique guideline and standard data set allows greater understanding. Our review showed that (75). Despite the rapid growth of technologies and health the effects variables such as environmental factors, information systems, most of health information systems political policies, exposure to infectious diseases during do not merge patients’ records with external datasets. pregnancy and nutritional status on maternal mortality This fact can explain why isolated data systems cannot are largely ignored. Evidence indicates important be used to recognize how the physical and environmental linkages between the water and sanitation environment context of each patient influences his/her health choices

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Table 2 Frequency of variables examined in the studies Background variables No. (%) (n = 40) Maternal factors Maternal age 11 (27.5) Antepartum haemorrhage 1 (25.0) Antenatal care visits 5 (12.5) Use of contraception (family planning) 2 (5.0) Number of children 1 (25.0) Parity 5 (12.5) Newborn outcomes 1 (25.0) Complications during last pregnancy 1 (25.0) Gestational age 2 (5.0) Birth weight 4 (10.0) Multiple births 2 (5.0) Type of delivery (normal or caesarean section, emergency or elective) 3 (7.5) Birth order and interval 3 (7.5) Socioeconomic factors Educational level of pregnant woman 10 (25.0) Parents’ educational level 3 (7.5) Household wealth 9 (22.5) Mother’s ethnicity 3 (7.5) Mother’s occupation 2 (5.0) Women’s autonomy within society 3 (7.5) Marital status 4 (10.0) Employment of head of household (employed/unemployed) 1 (25.0) Sex of head of household 1 (25.0) Sex of the newborn 2 (5.0) Sex of infants who have died 1 (25.0) Religion 1 (25.0) Exposure to media 2 (5.0) Exposure to family planning messages 1 (25.0) Residential area(urban, rural) 9 (22.5) Year of birth of mother 1 (25.0) Health care service factors Human resources 3 (7.5) Maternity and delivery beds 2 (5.0) Type of facility 4 (10.0) Level of delivery care (basic or comprehensive) 3 (7.5) Readiness of facilities to provide good delivery care 1 (25.0) Type of birth attendant (skilled or traditional) 2 (5.0) Place of delivery 3 (7.5) Ecological determinant factors Level of social vulnerability in catchment area 1 (25.0) Proportion of indigenous people in catchment area 1 (25.0) Environmental factors Drinking-water quality 1 (25.0) Health-related factors Chronic diseases (high blood pressure, diabetes, heart disease) 2 (5.0) Smoking and tobacco use during pregnancy 2 (5.0) Alcohol use during pregnancy 1 (25.0) HIV 1 (25.0)

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Table 2 Frequency of variables examined in the studies (Concluded) Background variables No. (%) (n = 40) Geographic factors visualized on GIS Season of birth 3 (7.5) Distance to facility 16 (40.0) Travel time to facility and emergency obstetric care 17 (42.5) Type of transport taken to facility (on foot, vehicle, ambulance) 4 (10.0) Distribution health services and emergency obstetric care facilities per population 11 (27.5) Distribution of human resources 1 (25.0) Childbirths per region at health facilities, at home, or outside home or health facility (e.g. in 5 (12.5) car/ambulance) Distribution of childbirths occurring unassisted by health professionals 1 (25.0) Distribution of early neonatal, early fetal and late fetal deaths 4 (10.0) Distribution of woman receiving antenatal care 2 (5.0) Distribution of women who had caesarean sections 2 (5.0) Distribution of women of reproductive age 2 (5.0) Distribution of private and public maternity units 1 (25.0) Distribution of maternity beds 1 (25.0) Distribution of women with high-risk pregnancies 1 (25.0) Distribution of births with poor neonatal outcomes (national) 1 (25.0) Distribution of facility-based peripartum fetal care 1 (25.0)

and health outcomes. Therefore, the use of tools such as searched only two databases which is another limitation GIS is needed to evaluate these associations. Pregnant as there might have been some relevant articles published women’s access to health care centres and improvement in other languages and included in other databases. in their health status are basic rights of women and can be thought of as an index of development in any country. Conclusion Our study had some limitations. First, the variables examined in some of the studies were not clearly reported Our review highlights the various applications of GIS in and may have been missing. Second, we classified the examining important variables in maternal care, and the extracted variables based on expert consensus for a need for programmes to improve the accessibility, use better reporting. As such, we may have misclassified and quality of care for pregnancy and childbirth. Health some variables. Third, although we reported the effect care planners can use GIS to determine the best location of these variables on maternal care, we could not and capacity of new health care facilities, and assess the undertake a precise analysis because of the large number costs. Furthermore, electronic health technologies, such of descriptive studies and the many different objectives as telemedicine, may be a way to overcome barriers of of the studies. We only included articles in English and geographic access.

Acknowledgement We thank Dr Reza Khajouei and Dr Khodadad Sheikhzadeh for their comments. Funding: None. Competing interests: None declared.

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Application des systèmes d’information géographique à la santé maternelle : étude exploratoire Résumé Contexte : L ’ amélioration de la santé maternelle est une priorité sanitaire à l’échelle mondiale et nécessite une évaluation précise des facteurs qui influent sur la santé des mères. Des systèmes d’information géographique ont été utilisés pour étudier les problèmes de santé maternelle. Objectifs : La présente étude avait pour objectif d’identifier les travaux de recherche faisant appel aux systèmes d’information géographique dans le domaine des soins de santé maternelle et de déterminer les variables en matière de santé et de mortalité maternelles que ces systèmes permettent de faire apparaître. Méthodes : Il s’agissait d’une étude exploratoire dans laquelle nous avons systématiquement recherché dans PubMed et Science Direct des études qui utilisaient des systèmes d’information géographique pour évaluer les soins de santé maternelle. Nous avons inclus toutes les études transversales pertinentes publiées en anglais entre décembre 1995 et décembre 2017. Nous avons extrait de chaque étude les informations suivantes : année d’étude, région, objectifs, type de système d’information géographique utilisé, variables mises en évidence par le système d’information géographique, et toutes les autres variables examinées concernant la santé maternelle. Résultats : Sur 5240 articles initialement récupérés, 40 ont fait l’objet d’une analyse détaillée. La plupart des études (n = 32) ont été réalisées dans des pays en développement en Afrique, en Asie, en Amérique latine et dans les Caraïbes. Grâce aux systèmes d’information géographique, la plupart des études (n = 33) ont permis de faire ressortir la distance entre le lieu d’habitation des mères et les établissements de santé ainsi que le temps de trajet pour se rendre dans les centres de soins. Les autres facteurs examinés portaient sur les capacités en matière de soins prénatals (n = 4) et de santé maternelle (n = 3). Conclusions : Il n’existe pas de recherche exhaustive sur l’application des systèmes d’information géographique aux soins maternels. La plupart des études ont appliqué une cartographie descriptive simple des schémas de répartition spatiale, complétée par l’ajout de quelques variables pertinentes.

تطبيق ُن ُظم املعلومات اجلغرافية يف جمال صحة األم: استعراض استكشايف ليىل أمحديان، فاطمة صاحلي، قمبيز هباء الدين بيجي اخلالصة اخللفية: ُعد يحتسني صحة األم أولوية صحية عىل الصعيد العاملي، ويتطلب ًتقييام ً دقيقاللعوامل التي تؤثر عىل صحة األم. وقد ُاست ِخدمت ُنظم املعلومات اجلغرافية الستكشاف املشاكل املتعلقة بصحة األم. األهداف: هدفت هذه الدراسة إىل حتديد الدراسات التي تستخدم ُظم ناملعلومات اجلغرافية يف جمال الرعاية الصحية لألمهات، وحتديد متغريات صحة األم َوو َف َيات األمهات التي ُتظهرها هذه ُالنظم. طرق البحث: كان هذا ًاستعراضا ًاستكشافيا بحثنا فيه ٍ بأسلوبمنهجي يف قواعد بيانات PubMed وScience Direct عن الدراسات التي تستخدم ُظم ناملعلومات اجلغرافية لتقييم الرعاية الصحية لألمهات. وأدرجنا مجيع الدراسات املقطعية وثيقة الصلة املنشورة باللغة اإلنجليزية يف الفرتة بني ديسمرب/كانون األول 1995وديسمرب/كانون األول 2017. واستخلصنا املعلومات التالية من مجيع الدراسات ُامل َدرجة: سنة الدراسة، واإلقليم، واألهداف، ونوع نظام املعلومات اجلغرافية َ م،املستخد واملتغريات التي ُظهرها ينظام املعلومات اجلغرافية، ومجيع املتغريات األخرى التي درسناها واملتعلقة بصحة األم. النتائج: ُأدرجت 40مقالة لالستعراض التفصييل من أصل 5240 مقالة اس ُرتجعت يف البداية. ُوأجريت معظم الدراسات )العدد = (32 يف بلدان نامية يف أفريقيا وآسيا وأمريكا الالتينية ومنطقة البحر الكاريبي. وأظهرت معظم الدراسات )العدد = 33( ُبعد األمهات عن املرافق الصحية ووقت السفر إىل مراكز الرعاية الصحية يف ُن ُظم املعلومات اجلغرافية. وشملت العوامل األخرى التي خضعت للدراسة القدرة عىل تقديم الرعاية السابقة للوالدة )العدد = 4(، والقدرة عىل تقديم اخلدمات الصحية لألمهات )العدد = 3(. االستنتاجات: ال توجد بحوث شاملة بشأن تطبيق ُظم ناملعلومات اجلغرافية يف جمال رعاية األمهات. َّوطبقت معظم الدراسات رسم خرائط وصفية بسيطة ألنامط التوزيع املكاين مع ٍعدد ٍقليل من املتغريات.

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Reproductive and behavioural risk factors of low birth weight among newborns in Al Thawra Hospital, Sana’a, Yemen

Idayu Idris,1 Manal Sheryan,1,2 Qistina Ghazali1 and Azmawati Nawi1

1Department of Community Health, Faculty of Medicine, UKM Medical Centre, Cheras, Kuala Lumpur, Malaysia (Correspondence to: A. Nawi: azma- [email protected]). 2Al Thawra Hospital, Sana’a, Yemen.

Abstract Background: Low birth weight can lead to infant death, especially during the first year of life. Aims: To assess risk factors related to low birth weight babies in Sana’a, Yemen. Methods: We conducted an unmatched case–control study of 252 women who came for delivery at Al Thawra Hospital, Sana’a, Yemen, between August and October 2016. Results: Significant risk factors for low birth weight were: birth interval < 2 years; history of pre-eclampsia during current pregnancy; preterm gestational age < 37 weeks; and khat chewing or smoking during pregnancy. After controlling for all the confounders, only birth interval < 2 years was significantly associated with low birth weight. Conclusion: Shorter birth interval is an important risk factor for low birth weight; therefore, improving maternal awareness of this should be emphasized during postnatal follow-up. Keywords: low birth weight, prematurity, pre-eclampsia, khat chewing, smoking. Citation: Idris I; Sheryan M; Ghazali Q; Nawi A. Reproductive and behavioural risk factors of low birth weight among newborns in Al Thawra Hospital, Sana’a, Yemen. East Mediterr Health J. 2020;26(11):1415-1419. https://doi.org/10.26719/emhj.20.061 Received: 14/05/19; accepted: 27/11/19 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 teria, that is, women who gave birth to a single live infant and who were resident in Sana’a City for at least 1 year. Low birth weight (LBW) is defined as birth weight Women who had given birth to newborns weighing < 2.5 < 2.5 kg (1). Two main factors cause LBW: preterm deliv- kg were classified as cases, and women who had given ery (< 37 weeks’ gestation) and growth restriction, or a birth to newborns weighing ≥ 2.5 kg were classified as combination of both (2). LBW is related to maternal bi- controls. Exclusion criteria were newborns that weighed ological, social and general health (3). Infants with LBW < 1.5 kg or > 4.0 kg, twins, stillbirths, and infants with a have almost 20 times greater risk of dying compared visible congenital anomaly. From the medical records, to normal-weight newborn infants (4). LBW is predic- cases were selected by convenience sampling while con- tive of a newborn’s health and survival, and can lead to trols were selected by simple random sampling. All new- death during the first year of life. Unfortunately, even if borns were weighed within 1 hour after birth. Sample an LBW infant survives, they may face life-threatening size was calculated using Open Epi version 3.01 using a conditions throughout their life and be exposed to chron- formula one proportion. Based on a previous study in Su- ic health issues in later life (4). According to the World dan, with a prevalence of LBW of 12.6% (7), the sample size Health Organization (WHO), there are an estimated 25 calculated for this study was 252 mothers of newborns million LBW infants born each year worldwide, which comprise 17% of all live births, and about 95% of them are (126 cases and 126 controls). born in developing countries (5). Data collection There is a high prevalence of LBW infants in Yemen, Data were collected from selected women through self-ad- where 32% of all newborn infants have LBW (6). This study ministered questionnaires and medical records. Ques- was conducted to assess the maternal sociodemographic, tionnaires were administered via face-to-face interview reproductive and lifestyle risk factors related to LBW in and questions were closed-ended in nature (Yes/No an- Sana’a City, Yemen. swers). The questionnaires and medical records consisted of women’s age, educational level, occupational status, Methods birth parity, birth interval, history of previous abortion, history of pre-eclampsia during the current pregnancy, Study design and sampling gestational age of the newborn, number of antenatal care This was an unmatched case–control study conducted visits, as well as khat chewing and smoking during the at Al Thawra Modern General Hospital, located in Sana’a current pregnancy. Interviews were conducted by 2 well- City, Yemen during August–October 2016. This hospital is trained female data collectors within the first 24 hours af- one of the biggest referral hospitals in Yemen. The cases ter delivery, and medical record data were extracted after and controls were selected according to the inclusion cri- the interview. The researchers trained the data collectors

1415 Short research communication EMHJ – Vol. 26 No. 11 – 2020 and supervised them during data collection and checked 13 (10.3%) worked outside the home. There was no signif- all the questionnaires to ensure accuracy. icant association between cases and controls concerning sociodemographic and socioeconomic characteristics. Ethical considerations Birth interval < 24 months, history of pre-eclampsia, The study was approved by the Medical Research and preterm delivery, chewing khat, and smoking were Ethics Committee of the University of Science and Tech- significant risk factors for LBW (Tables 2 and 3). However, nology, Sana’a, Yemen. Before starting the interview, in multivariate analysis, the only significant risk factor the participants were informed about the purpose of the for LBW was birth interval < 24 months (aOR = 2.24, 95% study and its benefits. Verbal and signed consent were CI = 1.017–4.952, P = 0.045) after controlling for the effect obtained from the participants before data collection. The of other predictors. respondents were assured that all the information would be confidential and only used for this study. Discussion Statistical analysis LBW is a significant cause of morbidity and mortality All the data were analysed by SPSS version 24.0. Qualita- among neonates and children (8). Infants’ gestational tive variables were described by calculation of frequency, age has a vital role in determining BW. There is an in- and quantitative variables were represented by mean and creased risk of LBW for premature infants (< 37 weeks’ standard deviation. Odds ratios (ORs) and 95% confidence gestation). According to WHO, prematurity is the cause intervals (CIs) were calculated to measure the risk. χ2 and of LBW in about one third of LBW infants (8). The pres- Fisher’s exact tests were used to show significant asso- ent study showed that LBW was significantly associated ciations between cases and controls, as well as associa- with preterm delivery, which was consistent with pre- tion of various risk factors and LBW. We used multiple vious studies (5,7,8). The reason for this might be that logistic regression to calculate the adjusted ORs (aORs) most of the fetal growth and weight gain is in the late after controlling for all possible confounders, with the period of pregnancy; thus, preterm infants receive few- corresponding 95% CIs, for LBW concerning exposure of er nutrients, which can lead to LBW. In this study, khat interest. chewing during pregnancy was a significant risk factor for LBW, which was consistent with other studies (9,10). This might be due to the influence of khat on reducing Results maternal food intake, which affects proper weight gain A total of 126 cases and 126 controls were included in the during pregnancy and fetal growth. Smoking during study (Table 1). The mean age in the cases and controls pregnancy was a significant risk factor for LBW, which is was 25.9 (standard deviation; 7.06) and 25.2 (5.48) years, supported by most studies worldwide (11,12). The harmful respectively. Most cases and controls were aged 20–29 components of cigarettes or hubble-bubble get into the years. In the case group, 67 (53.2%) women did not com- maternal circulation and then to the placenta, affecting plete their primary education and 59 (46.8%) who did. In fetal growth and weight. the control group, 58 (46%) women did not complete their Recommendations can be made to reduce the primary education and 68 (54%) did. In terms of occupa- prevalence of LBW. Screening should be conducted by tion, 116 (92.1%) women in the case group were house- healthcare professionals of pregnant women with high wives and 10 (7.9%) worked outside the home. In the risks of delivering LBW infants, especially if the mothers control group, 113 (89.7%) women were housewives and have a birth interval < 24 months. Furthermore, awareness

Table 1 Maternal sociodemographic characteristics of study participants Sociodemographic characteristics Cases, n = 126 Controls, n = 126 P* OR 95% CI Mean n % Mean n % (SD) (SD) Age (years) 25.92 (7.06) 25.26 (5.48) < 20 21 16.7 17 13.5 0.301 1.45 0.71–2.96 20–29 70 55.6 82 65.1 Ref ≥ 30 35 27.8 27 21.4 1.52 0.84–2.75 Educational level Did not complete basic education 67 53.2 58 46.0 0.257 1.33 0.81–2.18 Completed basic education and more 59 46.8 68 54.0 Ref Occupational status Housewife 116 92.1 113 89.7 0.512 1.33 0.56–3.17 Work outside 10 7.9 13 10.3 Ref *2 Statistically significant at P < 0.05. CI = confidence interval; OR = odds ratio; SD = standard deviation.

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Table 2 Maternal reproductive factors for low birth weight Reproductive factors Cases, n = 126 Controls, n = 126 P OR 95% CI n % n % Birth parity 1 57 45.2 50 39.7 0.655 1.19 0.60–2.36 2 23 18.3 24 19.0 Ref 3 or more 46 36.5 52 41.3 0.92 0.46–1.85 Birth interval < 24 months 33 47.8 20 26.7 0.009* 2.52 1.26–5.06 ≥ 24 months 36 52.2 55 73.3 Ref History of abortion Yes 27 21.4 23 18.3 0.527 1.22 0.66–2.27 No 99 78.6 103 81.7 Ref History of pre-eclampsia Yes 27 21.4 10 7.9 0.002* 3.16 1.46–6.86 No 99 78.6 116 92.1 Ref Gestational age Preterm (< 37 weeks) 38 30.2 1 .8 < 0.001* 53.98 7.27–400.53 Full term 88 69.8 125 99.2 Ref No. of antenatal care visits < 4 44 34.9 35 27.8 0.222 1.40 0.82–2.38 ≥ 4 82 65.1 91 72.2 Ref *χ2 Statistically significant at P < 0.05. CI = confidence interval; OR = odds ratio.

Table 3 Lifestyle risk factors for low birth weight Lifestyle risk factors Cases Controls P OR 95% CI n % n % Khat chewing Yes 83 65.9 66 52.4 0.029* 1.76 1.06–2.92 No 43 34.1 60 47.6 Ref Smoking Yes 41 32.5 17 13.5 < 0.001* 3.09 1.64–5.82 No 85 67.5 109 86.5 Ref *χ2 Statistically significant atP < 0.05. CI = confidence interval; OR = odds ratio. raising and health education on how to carry on a healthy Conclusion pregnancy should be focused individually. Improvement Risk factors for LBW identified in this study can be re- of lifestyle by all means, and avoiding smoking and duced and prevented by improving maternal health edu- chewing khat during pregnancy are essential. Pregnant cation, especially on pregnancy spacing. women need access to suitable maternal health services, including antenatal care and nutritional counselling Funding: None services. Competing interests: None declared.

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Facteurs de risque reproductifs et comportementaux liés au faible poids de naissance chez les nouveau-nés de l’hôpital Al Thawra de Sanaa au Yémen Résumé Contexte : Un faible poids de naissance peut entraîner la mort du nourrisson, en particulier pendant la première année de vie. Objectifs : La présente étude visait à évaluer les facteurs de risque liés au faible poids de naissance des enfants nés à Sanaa au Yémen. Méthodes : Nous avons mené une étude cas-témoins non appariés auprès de 252 femmes venues accoucher à l’hôpital Al Thawra de Sanaa, au Yémen, entre août et octobre 2016. Résultats : Les facteurs de risque significatifs du faible poids de naissance étaient un intervalle entre deux naissances inférieur à deux ans, des antécédents de pré-éclampsie pendant la grossesse concernée, l’âge gestationnel prématuré inférieur à 37 semaines et la consommation de khat ou le tabagisme pendant la grossesse. Après contrôle de tous les facteurs de confusion, seul un intervalle entre deux naissances inférieur à deux ans était significativement associé à un faible poids de naissance. Conclusion : La réduction de l’intervalle entre les naissances représente un facteur de risque important de faible poids de naissance ; par conséquent, il convient de mettre l’accent sur une meilleure sensibilisation des mères sur ce point à l’occasion du suivi postnatal.

عوامل اخلطر اإلنجابية والسلوكية النخفاض وزن املواليد يف مستشفى الثورة يف صنعاء باليمن إيدايو إدريس، منال رشيان، قستينا غزايل، أزماوايت ناوي اخلالصة اخللفية: يمكن أن يؤدي انخفاض الوزن عند الوالدة إىل وفاة ُالر َّضع، وخاصة خالل السنة األوىل من أعامرهم. األهداف: هدفت هذه الدراسة إىل تقييم عوامل اخلطر املتعلقة باألطفال املصابني بانخفاض الوزن عند الوالدة يف صنعاء باليمن. طرق البحث: أجرينا دراسة حاالت وشواهد فريدة من نوعها ملا جمموعه امرأة252 حرضن للوالدة يف مستشفى الثورة يف صنعاء باليمن، يف الفرتة بني أغسطس/آب وأكتوبر/ترشين األول 2016. النتائج: ِمن بني عوامل اخلطر املهمة لإلصابة بانخفاض الوزن عند الوالدة ِّتدن الفرتة الفاصلة بني مرات الوالدة إىل أقل من َعام ْني؛ ووجود تاريخ سابق ملقدمات تسمم احلمل أثناء احلمل احلايل، والعمر َاحل ْميل املبكر الذي يقل عن 37 ً، أسبوعاومضغ القات أو التدخني أثناء احلمل. وبعد السيطرة عىل مجيع عوامل اإلرباك، مل يكن هناك ارتباط مهم سوى بني ِّتدن الفرتة الفاصلة بني مرات الوالدة إىل أقل من َعام ْني وانخفاض الوزن عند الوالدة. االستنتاجات: ُي َعد ِقرص الفرتة الفاصلة بني مرات الوالدة عامل خطر ً مهاملنقص الوزن عند الوالدة؛ ولذا، ينبغي التأكيد عىل تعزيز وعي األمهات هبذا األمر أثناء متابعة ما بعد الوالدة.

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8. Sutan R, Mohtar M, Mahat AN, Tamil AM. Determinant of low birth weight infants: a matched case control study. Open J Prev Med. 2014;4:91–9. 9. Demelash H, Motbainor A, Nigatu D, Gashaw K, Melese A. Risk factors for low birth weight in Bale zone hospitals, South-East Ethiopia: a case–control study. BMC pregnancy and childbirth. 2015 Oct 13;15:264. http://dx.doi.org/10.1186/s12884-015-0677-y PMID:26463177 10. Abdel-Aleem MA. Khat chewing during pregnancy: an insight on an ancient problem impact of chewing khat on maternal and fetal outcome among Yemeni pregnant women. J Gynaecol Neonat Biol. 2015; http://dx/doi.org/10.15436/2380-5595.15.004 11. Zheng W, Suzuki K, Tanaka T, Kohama M, Yamagata Z, Okinawa Child Health Study Group. Association between maternal smoking during pregnancy and low birthweight: effects by maternal age. PLoS One. 2016 Jan 21;11(1):e0146241. http://dx.doi. org/10.1371/journal.pone.0146241 PMID:26795494 12. Stojanović M, Bojanić V, Musović D, Milosević Z, Stojanović D, Visujić A et al. Maternal smoking during pregnancy and socioeconomic factors as predictors of low birth weight in term pregnancies in Niš. Vojnosanit Pregled. 2010 Feb;67(2):145–50 (in Serbian) http://dx.doi.org/10.2298/vsp1002145s PMID:20337097

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Barriers to the use of dental services by children in Lebanon and association with parental perception of oral health care

Ingrid Karam,1 Miran A. Jaffa2 and Joseph Ghafari1

1Division of Orthodontics and Dentofacial Orthopedics, Department of Otorhinolaryngology, Head and Neck Surgery, American University of Beirut Medical Center, Beirut, Lebanon. 2Epidemiology and Population Health Department, Faculty of Health Sciences, American University of Beirut, Beirut, Lebanon. (Correspondence to: Miran Jaffa: [email protected]).

Abstract Background: Oral health is important to general health but use of dental services varies considerably, particularly for children. Aims: We aimed to determine factors associated with parents’ use of dental services for their children in Lebanon, and their perception of dental care relative to medical care. Methods: A convenience sample of public and private schools in Beirut was selected between January and May 2013. Parents of children in grades 2–6 (aged 7–12 years) were invited to complete a questionnaire covering socioeconomic characteristics and use of dental services. Logistic regression analysis was used to assess the relationship between use of dental services, and parents’ socioeconomic characteristics and awareness and perceptions of dental services. Results: The parents of 316 children returned the questionnaire. Most children (72.8%) had been taken to the dentist in the past year, mainly for emergency care. Most parents (78.2%) considered dental care as important as or more important than medical care, and 89.9% were willing to contribute to dental insurance. Use of dental services was significantly associated with: older age of the parent (odds ratio, OR = 1.04; 95% confidence interval, CI: 1.02–1.06); awareness of dental care centres offering affordable treatment (OR = 3.18; 95% CI: 1.52–6.68); and children being in private schools (OR = 2.00, 95% CI: 1.08– 3.95). It was negatively associated with > 4 children in the family compared with 1 child (OR = 0.18; 95% CI: 0.04–0.81). Conclusion: Barriers to dental care for children were mostly related to economic factors. Keywords: dental care for children, oral health care, dental insurance, Lebanon Citation: Karam I; Jaffa MA; Ghafari J. Barriers to the use of dental services by children in Lebanon and association with parental perception of oral health care. East Mediterr Health J. 2020;26(11):1420–1424. https://doi.org/10.26719/emhj.20.079 Received: 02/05/19; accepted: 03/11/19 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 care. Although a statistically significant association has been reported between perceived general and dental Poor oral health, which is related to excessive sugar in- health (14), the relationship between such perception and take and low levels of fluoride exposure (1,2), affects use of dental services is not well known. 60–90% of schoolchildren globally (3) and the most so- cially disadvantaged populations (4), particularly given We hypothesized that the perception of the the high cost of treatment in low- and middle-income importance of oral care in relation to medical care countries (5,6). The use of dental services has been widely may be associated with use of dental services, and that investigated in relation to sociodemographic variables. utilization among Lebanese schoolchildren would reflect Utilization is lower in younger people (21–35 years) and the oral care perception of parents and related practices. Private and public schools are fairly equally distributed people of lower socioeconomic status (7). On the other in Beirut – 52.8% and 47.2% of pupils attend private and hand, the use of dental services in children is greater public institutions, respectively (15). They therefore when parents have a higher education (4,7,8) and have represent a good model for socioeconomic background. a better perception about oral health, including preventive and comprehensive care rather than only emergency The aims of our study were to: (i) identify the factors treatment (e.g. toothache) (4,9). In addition, utilization of associated with access to dental care in schoolchildren dental care is greater when third-party dental coverage from different socioeconomic backgrounds and with is available – uninsured people are twice as likely to ne- the barriers preventing parents from using needed glect dental care as insured people (10). Low utilization of dental services for their children; and (ii) assess parental dental services was associated with treatment expenses perception of dental care in relation to medical care. in Lebanon (11), where only about 20% of the population benefit from dental insurance through military and civil Methods servant programmes (12). In addition, oral health is globally the most common Study design and sample unmet health care need (13). This fact raises the question This was a cross-sectional study of children in grades 2 to about people’s perception of oral care in relation to medical 6 (aged 7–12 years) attending five private and two public

1420 Short research communication EMHJ – Vol. 26 No. 11 – 2020 schools in Beirut that agreed to allow children and their computation of standard errors. Data are presented as parents to participate in the study. The sample was a con- unadjusted and adjusted odds ratios (OR) and 95% convenience sample in the first phase (January–May 2013) fidence intervals (CI). Stata, version 12.1 was used for the of a multiphase study on the children’s oral health. In analyses. this phase, the children were given a consent form and a questionnaire to take home to their parents for them Ethical considerations to sign and complete within one week. Parents who re- The multiphase study was approved by the Institutional turned the signed consent form and the completed ques- Review Board of the American University of Beirut. All tionnaire were included in the study. participating parents signed an informed consent form. Power analysis showed that with a sample size of 316 responses, an effect size of 0.07 (between a small (0.02) Results and the medium (0.15) effect size) and a probability level of 0.05, the statistical power is 0.8, with 20 predictors. The parents of 316 children in grades 2 to 6 (aged 7–12 years) returned the questionnaire and signed the in- Data collected formed consent form. Age was recorded for 273 (86.4%) The questionnaire included standard demographic and parents: mean age and standard deviation (SD) was socioeconomic questions and questions on the use of 38.30 (SD 6.40) years, range 16–57 years. The mean age dental services. It did not include any scale that required of the children was 9.5 (SD 1.5) years. The proportion of validation. We did a pilot study on a random sample of completed questionnaires was about the same for public 10 parents to ensure that the questions were clear to the (n = 151, 47.8%) and private (n = 165, 52.2%) schools. participants. We excluded these parents from the study Most parents (n = 230; 72.8%) had taken their children to avoid introducing bias. The recorded categorical var- to the dentist at least once in the past year, 61.3% of whom iables were: (n = 141/230) had made more than one visit. The reasons · Outcome variable: use of dental services – parents for the visits were: decay and acute pain (n = 206; 89.6%), had taken their children to the dentist in the past year regular check-up (n = 153; 66.5%) and appearance of teeth (yes/no) and reasons for taking them to the dentist (n = 131; 57.0%). Most parents (n = 284; 89.9%) were willing (routine check-up and prevention, emergency moti- to invest in dental health and increase their utilization vated by pain, or orthodontics). of dental services if costs were covered by dental insurance. We found statistically significant associations · Sociodemographic characteristics – sex of the re- between use of dental services and eight variables in sponding parent, marital status (married/separated/ the simple regression analysis (Table 1): respondent’s divorced), respondent parent’s educational level (read age, respondent’s educational level, number of children and write, primary school, middle and secondary in family, monthly family income, school type, medical school, college/university), number of children in the insurance, perception of oral and general health, and family (1,2,3,4, > 4). awareness of the presence of dental care centres. · Socioeconomic characteristics: family monthly in- Sex (P = 0.481) and marital status (P = 0.705) were not come (< 1 , ≥ 1 million Lebanese pounds (US$ 1 = 1500 significantly associated with use of dental services and Lebanese pounds]), children’s school (public or pri- were not included in the multivariable analysis. In the vate), family medical/dental insurance (yes/no). multivariable analysis, four of these variables remained · Respondent parent’s awareness of dental care centres significantly associated with use of dental services – use offering affordable treatment (yes/no). of dental services increased with the older age of the respondent parent, fewer children in the family (> 4 · Respondent parent’s perception of their children’s children was significant in the unadjusted and adjusted oral health (less/equally/more important than their analysis), awareness of dental care centres offering general health). affordable treatments, and children being in private · Respondent parent’s willingness to use dental servic- schools (Table 1). es more for their children if they were covered by or paid premiums towards dental insurance (yes/no). Discussion Statistical analysis Many of our results corroborate the findings of previ- We used simple and multivariable logistic regression ous studies. For example, the most common reason for analyses to evaluate the association between use of den- dental visits was emergency care (acute pain and decay) tal services and the independent variables. Variables that rather than preventive care and orthodontics (16), and were statistically significant (P < 0.05) in the simple logis- use of dental services was associated with economic tic regression analysis were entered in the multivariable status, educational level of the parent, and monthly fam- analysis. Given that observations from the same school ily income (4,7–17). However, our main results relate to tend to be correlated, we used a logistic regression anal- the effect on behaviour of awareness of affordable den- ysis with a cluster effect at the school level. This method tal centres and the perception that dental care is equal- incorporates within-school intracluster correlation in the ly important as or more important than medical care.

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Table 1 Simple and multivariable logistic regressions for dental services utilization adjusted for intracluster correlation Variable Values Unadjusted OR P Adjusted ORa P (95% CI) (95% CI) Mean (SD) Respondents’ age (years) 38.30 (6.40) 1.04 (1.02–1.07) < 0.001 1.04 (1.02–1.06) < 0.001 No. (%) Educational level Read and write/Primary (Ref) 74 (23.8) Intermediate/Secondary 94 (30.2) 0.93 (0.34–2.53) 0.901 1.02 (0.33–3.10) 0.967 College/University 143 (46.0) 1.86 (1.14–3.03) 0.013 1.32 (0.70–2.47) 0.385 Children in the family 1 (Ref) 12 (3.8) 2 102 (32.3) 0.34 (0.07–1.63) 0.180 0.55 (0.17–1.80) 0.328 3 113 (35.8) 0.22 (0.03–1.31) 0.097 0.33 (0.08–1.28) 0.111 4 58 (18.4) 0.18 (0.02–1.16) 0.072 0.24 (0.05–1.00) 0.050 > 4 31 (9.8) 0.18 (0.03–0.85) 0.031 0.18 (0.04–0.81) 0.025 Monthly family income (Lebanese poundsb) < 1 000 000 (Ref) 134 (44.8) ≥ 1 000 000 165 (55.2) 2.28 (1.42–3.66) < 0.001 1.63 (0.89–2.98) 0.108 School type Public (Ref) 151 (47.8) Private 165 (52.2) 2.69 (1.71–4.23) < 0.001 2.00 (1.08–3.95) 0.027 Have medical insurance No (Ref) 100 (33.0) Yes 203 (67.0) 1.99 (1.35–2.93) < 0.001 0.94 (0.54–1.65) 0.84 Perception of oral health compared with general health Less important (Ref) 52 (17.4) As important/more important 247 (82.6) 2.13 (1.01–4.52) 0.047 1.02 (0.01–1.65) 0.905 Awareness of dental care centres offering affordable services No (Ref) 157 (52.9) Yes 140 (47.1) 1.99 (1.25–3.19) 0.004 3.18 (1.52–6.68) 0.002 OR: odds ratio; CI: confidence interval; SD: standard deviation; Ref: reference category. aAdjusted for all other variables in the multivariable analysis. bUS$ 1 = 1500 Lebanese pounds. Percentages (%) are computed out of the total responses for each question

The fact that almost twice as many of the parents who had artificial split may lie in education (separate medical medical insurance used dental services for their children and dental schools) and insurance (separate for medical compared with those without medical insurance shows and dental needs) (19). Policy-makers should rethink that insurance coverage increases utilization, potential- this categorization and consider integration based on ly improving oral health and preventive care visits. This the principle that oral health is part of total health. The trend has been shown in low-income Americans with a financial burdens of dental services may be addressed dramatic increase (from 33% to 80%) in dental service uti- by giving greater coverage for preventive care and lization when they have medical insurance (18). Further- progressive copayment for different treatment options of more, most parents of children in both public and private more demanding procedures. schools (89.8%) were willing to invest in dental health, which shows the importance of implementing dental in- Our study has some limitations, mainly the potential surance within the medical insurance programmes. response bias and the convenience nature of the sample Health issues are concerned with life and death or (selection was based only on agreement of schools and quality of life. Most dental and many medical problems parents to participate in the study). More research is are not life-threatening but they can affect quality of warranted on perception and awareness of dental needs life considerably. Yet, oral health care and general health and care with a larger sample from different geographic care are considered independent entities. Why should areas. Such research should evaluate the psychological a line be drawn between a headache and a toothache, disposition to seek preventive dental care, and ways to whether mild or debilitating? The roots of a seemingly encourage everyone to have regular check-ups.

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In conclusion, the use of dental services reflected of total health and suggests that the present system of the disparity in economic and educational levels of the separate coverage for medical and dental needs should be parents. Even the poorer respondents would be prepared to reconsidered. share in the cost of dental insurance coverage, regardless Funding: None. of the presence or absence of medical insurance. This finding indicates that people perceive oral health as part Competing interests: None declared.

Recours aux services dentaires chez les enfants au Liban : obstacles et association avec la perception parentale des soins de santé bucco-dentaire Résumé Contexte : La santé bucco-dentaire est importante pour la santé générale, mais le recours aux services dentaires varie considérablement, en particulier chez les enfants. Objectifs : La présente étude visait à déterminer les facteurs associés au recours par les parents aux services dentaires nécessaires pour leurs enfants au Liban, et leur perception de ces soins par rapport aux soins médicaux. Méthodes : Un échantillon de commodité d’écoles publiques et privées de Beyrouth a été sélectionné entre janvier et mai 2013. Les parents d’enfants scolarisés en école primaire (âgés de 7 à 12 ans) ont été invités à remplir un questionnaire dans lequel ils devaient indiquer les caractéristiques socio-économiques et le recours aux services dentaires. L’analyse de régression logistique a été utilisée pour évaluer la relation entre le recours aux services dentaires et les caractéristiques socio-économiques des parents ainsi que la sensibilisation à ces services et la perception de ceux-ci. Résultats : Les parents de 316 enfants ont renvoyé le questionnaire. La plupart des enfants (72,8 %) avaient été emmenés chez le dentiste au cours de l’année précédente, principalement pour des soins d’urgence. La plupart des parents (78,2 %) considéraient que les soins dentaires étaient aussi importants ou plus importants que les soins médicaux, et 89,8 % étaient disposés à contribuer à l’assurance dentaire. Le recours aux services dentaires était associé de maniere significative à : un âge plus avancé du parent (odds ratio, OR = 1,04 ; intervalle de confiance à 95 %, IC : 1,02‐1,06) ; la connaissance de centres de soins dentaires offrant un traitement abordable (OR = 3,18 ; IC à 95 % : 1,52‐6,68) ; et à la scolarisation des enfants dans des écoles privées (OR = 2,00, IC à 95 % : 1,08‐3,95). Il y avait une corrélation négative dans les familles de plus de quatre enfants comparativement aux foyers à enfant unique (OR = 0,18 ; IC à 95 % : 0,04‐0,81). Conclusion : Les obstacles aux soins dentaires pour les enfants étaient principalement liés à des facteurs économiques.

استخدام األطفال خلدمات طب األسنان يف لبنان: العوائق التي حتول دون إدراك أمهية الرعاية الصحية للفم والعوامل املرتبطة بذلك إنجريد كرم، مران جافا، جوزف غفري اخلالصة اخللفية: حتظى صحة الفم بأمهية للصحة العامة، ولكن استخدام خدمات طب األسنان يتفاوت ًتفاوتا ًكبريا، ال ّامسي بالنسبة لألطفال. األهداف: هدفتهذه الدراسة إىل حتديد العوامل املرتبطة باستخدام اآلباء خلدمات طب األسنان الالزمة ألطفاهلم يف لبنان، ونظرهتم إىل رعاية األسنان بالنسبة للرعاية الطبية. طرق البحث:اختريت عينة عشوائية من املدارس العامة واخلاصة يف بريوت يف الفرتة بني يناير/كانون الثاين ومايو/أيار 2013. ُوو ِّجهت دعوة آلباء وأمهات األطفال يف الصفوف 2-6 )الذين ترتاوح أعامرهم بني 7- 12سنة( الستكامل استبيان ُم َّ م نظيتناول اخلصائص االجتامعية االقتصادية، واستخدام خدمات طب األسنان. ُواست ِمحتليل خداالنحدار اللوجستي لتقييم العالقة بني استخدام خدمات طب األسنان، واخلصائص االجتامعية االقتصادية، والوعي بخدمات طب األسنان والتصورات بشأهنا. النتائج: َّسلم آباء 316 ً طفالاالستبيان بعد استكامله. وقد ذهب معظم األطفال ) %( إىل72.7 طبيب األسنان يف العام املايض، ال ّسيام لتلقي الرعاية الطارئة. واعترب معظم اآلباء ) %( 78.2أن رعاية األسنان حتظى بأمهية الرعاية الطبية نفسها أو أكثر، وأعرب 89.8% منهم عن استعدادهم للمشاركة يف خدمات التأمني عىل األسنان. ويف التحليل املتعدد املتغريات، ارتبط استخدام خدمات طب األسنان ً ارتباطا ًإجيابيا ًملحوظا بام ييل: – ُّتقدم ُعمر أحد الوالدين )نسبة األرجحية: 1.04 بفاصل ثقة 95%: 1.02 1.06(، ومعرفة مراكز رعاية األسنان التي ِّ متقد ًعالجا ميسور التكلفة )نسبة األرجحية = 3.18 بفاصل ثقة 95%: 1.52– (، 6.68واألطفال امللتحقني باملدارس اخلاصة )نسبة األرجحية = 2.00، بفاصل

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ثقة 95%: 1.08–3.95(. وارتبط استخدام خدمات طب األسنان ًارتباطا ًسلبيا بوجود أكثر من 4أطفال يف األرسة ًمقارنة بطفل واحد )نسبة األرجحية = 0.18 بفاصل ثقة %95: 0.04–0.81(. االستنتاجات: ترتبط العوائق التي تعرتض رعاية األسنان لألطفال يف الغالب بعوامل اقتصادية.

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Profil épidémiologique d’une intoxication au méthanol, El Hajeb (Maroc)

Sanah Essayagh,1 Mariama Bahalou,2* Meriem Essayagh3 et Touria Essayagh4*

1Laboratoire Agroalimentaire et Santé, Faculté des Sciences et Techniques, Université Hassan 1er, Settat (Maroc). 2Délégation de la Santé, Meknès (Maroc). 3Faculté de Médecine et de Pharmacie, Université Mohammed V, Rabat (Maroc). 4Laboratoire Sciences et Technologies de la Santé, Institut Supérieur des Sciences de la Santé, Université Hassan 1er, Settat (Maroc) (Correspondance à adresser à : [email protected] (TE). *Ces auteurs ont apporté la même contribution au travail.

Résumé Contexte : l’intoxication au méthanol est un problème pertinent dans les pays en développement. Nous signalons une intoxication au méthanol qui s’est produite le 22 mai 2017 à El Hajeb (Maroc). Objectifs : décrire l’ampleur de l’intoxication, déterminer sa source et instaurer les mesures préventives nécessaires. Méthodes : nous avons mené une enquête transversale. Un questionnaire normalisé comprenant des données socio-économiques, les symptômes cliniques et l’heure de consommation a été administré en face à face aux cas. Des prélèvements biologiques ont été effectués pour analyse toxicologique et physico-chimique. Les données ont été saisies et analysées sur Epi Info version 7. Résultats : au total, 26 cas ont été colligés avec un âge moyen de 39,7 (écart type [ET] 11,1) ans et un sex ratio homme/ femme de 5,5. Tous les cas intoxiqués étaient de faible niveau socio-économique. La durée moyenne de latence entre consommation et apparition des symptômes était de 1,5 (ET 1) jours. Les symptômes signalés étaient les faibles troubles de la conscience chez 14 cas (53,8 %), les douleurs abdominales chez 10 cas (38,5 %), les céphalées chez neuf cas (34,6 %), les vomissements chez huit cas (30,8 %) et le coma chez sept cas (27,1 %). La létalité a été de 65 % et quatre cas ont développé une cécité. Les résultats de laboratoire ont confirmé la présence de méthanol dans le sang avec des valeurs supérieures à 0,6 g/L. La dose de méthanol dans la bouteille incriminée était de 217 g/L. Conclusion : la sensibilisation de la population au danger du méthanol est importante. Une sensibilisation des professionnels de santé aux signes cliniques et à la conduite à tenir face à une intoxication au méthanol est nécessaire. Citation: Essayagh S; Bahalou M; Essayagh M; Essayagh T. Profil épidémiologique d’une intoxication au méthanol, El Hajeb (Maroc). East Mediterr Health J. 2020;26(11):1425–1429. https://doi.org/10.26719/2020.26.11.1425 Mots-clés : méthanol, intoxication, El Hajeb Reçu : 01/10/19 ; accepté : 16/12/19 © Organisation mondiale de la Santé 2020 Certains droits réservés. La présente publication est disponible sous la licence Creative Commons Attribution – Pas d’utilisation commerciale – Partage dans les mêmes conditions 3.0 IGO licence (CC BY-NC-SA 3.0 IGO; https://creativecommons. org/licenses/by-nc-sa/3.0/igo ).

Introduction Dans le cadre d’une alerte, l’équipe de surveillance épidémiologique d’El Hajeb a informé le 22 mai 2017, à L’alcool à brûler contient des concentrations variables 10 h 30, l’équipe de Meknès du transfert aux urgences de méthanol. Ce dernier est utilisé dans les antigels des du Centre hospitalier préfectoral (CHP) de Meknès de automobiles et les solvants (1). Il est aussi utilisé comme quatre cas groupés présentant des troubles visuels, substitut de l’alcool éthylique dans plusieurs boissons des douleurs abdominales et des vomissements. Une alcoolisées frelatées dans la classe de faible niveau socio- enquête épidémiologique pour vérification des cas a été économique dans les pays en développement, surtout effectuée afin de confirmer l’existence d’une intoxication en cas de prohibition de l’alcool. Le méthanol peut collective, de décrire son ampleur, de déterminer sa être ingéré de manière accidentelle ou avec intention source et d’instaurer les mesures préventives. suicidaire, entraînant ainsi des intoxications sous forme isolée ou collective. À l’intérieur du corps, il est métabolisé en acide formique qui, sans traitement, entraîne la cécité Méthodes ou la mort. Les études montrent des létalités allant de 76 % à 89 % (2,3). Le méthanol peut également affecter le Site de l’enquête tissu cérébral. L’évolution de l’intoxication au méthanol Pays d'Afrique du nord, le Maroc a une population de est conditionnée par le degré d’acidose et le délai entre 33,8 millions d’habitants. Il se compose de 12 régions, l’exposition et l’instauration du traitement spécifique (1). dont celle de Fès-Meknès. Cette région est composée Les signes cliniques de l’intoxication au méthanol sont de neuf provinces, dont El Hajeb, qui regroupe 16 non spécifiques, aboutissant à un diagnostic et un communes et compte une population d’environ traitement tardifs, et à une surmortalité. Le traitement se 35 282 habitants (7). Elle dispose d’un hôpital provincial base soit sur l’administration d’éthanol pour obtenir une qui, en présence de cas sévères, transfère les patients à concentration constante d’éthanol d’environ 1g/L (4,5), l’hôpital provincial de Meknès ou au centre hospitalier soit sur l’hémodialyse pour épuration (5,6). régional (CHU) de Fès.

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Schéma d’étude et définition de cas Tableau 1 Caractéristiques des cas d’intoxication au méthanol, El Hajeb (Maroc), mai 2017 Nous avons mené une enquête transversale à visée descriptive. L’enquête s’est déroulée durant la période Caractéristiques Total allant 22 au 29 mai 2017. Elle a concerné Meknès- (n = 26) Nbre (%) El Hajeb-Fès. Un cas a été défini comme toute personne habitant El Hajeb, ayant consommé une Âge moyen (ans) 39,7 (ET 1,1) boisson alcoolisée et ayant présenté, entre le 17 et le Sexe 23 mai 2017, au moins l’un des signes suivants : troubles Masculin 22 (84,6) visuels, céphalées, vomissements, nausées, douleurs Féminin 4 (15,4) abdominales, altération de l’état général, troubles de Situation matrimoniale la conscience ou coma. Les cas ont été recensés à Non marié 21 (80,8) partir du registre des urgences de l’hôpital d’El Hajeb. Marié 5 (19,2) Une recherche active des cas a aussi été menée auprès de la population d’El Hajeb, en concertation Revenu mensuel (US$) avec les autorités locales. Un interrogatoire avec les < 150 26 (100,0) malades survivants ou leurs proches a été réalisé. Le ≥ 150 0 (0,0) suivi des cas a été effectué auprès des hôpitaux d’El Type de domicile Hajeb et de Meknès, et des services de réanimation et Sans domicile fixe 6 (23,1) d’ophtalmologie du CHU de Fès. Avec domicile fixe 20 (76,9) Épidémiologie descriptive Consommation d’alcool local Un questionnaire a été administré en face à face pour Oui 20 (76,9) recueillir des informations sur : 1) les données socio- Non 6 (23,1) démographiques ; 2) les signes cliniques ; 3) la date Toxicomanie de consommation de méthanol et d’apparition des Oui 18 (69,2) symptômes ; 4) le lieu de procuration de l’alcool ; Non 8 (30,8) 5) l’évolution du malade ; et 6) les complications. Le ET : écart type. fournisseur agréé et les cas ont été interrogés sur la procédure de préparation du méthanol. La police judiciaire d’El Hajeb a procédé à la saisie du lot de moyenne de latence entre consommation et apparition méthanol pour stopper l’épidémie et assurer l’analyse des symptômes était de 1,5 (ET 1) jour. Les cas ont toxicologique et physico-chimique. Les données ont été commencé à se produire le 20 mai pour atteindre analysées sur Epi Info version 7. le maximum le 21 mai avec 11 cas. Le dernier cas a Enquête toxicologique et physico-chimique été enregistré le 23 mai à 18 heures (Figure 1). Les Des prélèvements biologiques ont été effectués et symptômes les plus enregistrés étaient les suivants : envoyés pour analyse au Centre Antipoison et de faibles troubles de la conscience chez 14 cas (53,8 %), Pharmacovigilance. Le méthanol et l’éthanol ont été douleurs abdominales chez 10 cas (38,5 %), céphalées dosés par chromatographie en phase gazeuse (gas chez neuf cas (34,6 %), vomissements chez huit chromatography, GC) avec un détecteur à ionisation cas (30,8 %) et coma chez sept cas (27,1 %). Dix-sept de ﬂamme (flame ionisation detector, FID) couplée à un personnes sont décédées, soit une létalité de 65 %, et quatre échantillonneur automatique d’extraction en espace de tête (headspace, HS) (GC-FID-HS). La recherche des drogues a été réalisée par des méthodes immuno- Figure 1 Courbe épidémique de l’intoxication au méthanol, El chromatographiques. Hajeb (Maroc), 22 mai 2017

Considérations éthiques 13 Tous les participants avaient donné leur consentement 12 Arrivée du Saisie du lot consommé lot consommé informel verbal. Les tests de laboratoire ont été réalisés à 11 10 la suite d’un diagnostic de routine. 9 8 7 Résultats 6

Nombre de cas 5 Épidémiologie descriptive 4 Durant l’épidémie, 26 cas ont été identifiés. L’âge moyen 3 était de 39,7 (ET 11,1) ans, avec des extrêmes allant de 28 2 à 58 ans et un sex ratio homme/femme de 5,5. Tous les 1 20 21 22 23 patients étaient de faible niveau socio-économique, sans domicile fixe pour six cas (23,1 %) (Tableau 1). La durée Début des symptômes

1426 Report EMHJ – Vol. 26 No. 11 – 2020 ont développé une cécité, soit 15,4 % (Tableau 2). Vingt Tableau 2 Répartition des symptômes de l’intoxication au cas ont déclaré avoir consommé de l’alcool frelaté (alcool méthanol, El Hajeb (Maroc), mai 2017 préparé localement), qui provenait du même fournisseur Symptômes Fréquence (%) agréé d’El Hajeb. (n = 26) Enquête toxicologique et physico-chimique Faibles troubles de la conscience 14 (53,8) Douleurs abdominales 10 (38,5) Les résultats des trois prélèvements biologiques des patients ont révélé la présence de méthanol dans le Céphalées 9 (34,6) sang avec des valeurs de 0,7 g/L, 1,35 g/L et 1,94 g/L. Le Vomissements 8 (30,8) niveau d’éthanol dans le sang était inférieur à 0,1 g/L. Coma 7 (27,1) Les prélèvements d’urine ont révélé la consommation de cannabis chez un malade (59 mg/mL). Les flacons Polypnée 6 (23,1) d’alcool toxique saisis par la police ont montré des Troubles visuels 5 (19,2) concentrations de méthanol de 217 g/L, 7 g/L et 6 g/L. Cécité 4 (15,4) Irritabilité 4 (15,4) Discussion L’intoxication au méthanol est un problème dans les pays en développement. Au Maroc, une intoxication latence comprise entre 9-24 heures en moyenne et liée à au méthanol a eu lieu en 1996 avec 76 cas, dont sept la dose ingérée ; la phase de symptomatologie initiale de décès et quatre cas de cécité (8-11). La majorité des cas l’intoxication qui est peu spécifique et qui est marquée d’intoxication au méthanol résultent d’une ingestion/ par des troubles neurologiques, des signes digestifs et inhalation ou d’une absorption transcutanée (12). La dose une polyurie associée à une polydipsie ; et la phase d’état létale est de 1 mL/kg (13). La dose toxique de méthanol où le méthanol ingéré est oxydé au niveau hépatique dépend de l’individu et du traitement reçu. Une en formaldéhyde et en acide formique par des enzymes. concentration de méthanol dans le sang supérieure à L’accumulation de l’acide formique est responsable de la 500 mg/L est associée à des toxicités graves alors qu’une toxicité et sa concentration est en lien avec la morbidité, concentration supérieure à 1500-2000 mg/L entraîne la la mortalité et la profondeur de l’acidose métabolique mort chez les patients non traités (14). observée dans l’intoxication au méthanol (17). Cet Dans notre étude, les trois patients pour lesquels des intervalle libre de plusieurs heures entre l’ingestion du prélèvements biologiques ont pu être effectués et chez méthanol et l’apparition des signes cliniques explique le qui les valeurs du méthanol dans le sang étaient de 0,7 g/L, retard dans la prise en charge des cas et la létalité élevée. 1,35 g/L et 1,94 g/L sont décédés. Ceci pourrait expliquer la À cela pourrait s’ajouter le manque de connaissances de létalité élevée dans notre étude. Dans l’enquête, tous les la part des professionnels de santé sur la conduite à tenir cas étaient de faible niveau socio-économique, ce qui est face à une intoxication au méthanol. compatible avec la littérature (15). Dans notre étude, on a constaté une prédominance masculine. Ceci pourrait être expliqué par le contexte marocain où seule une minorité Limites de l’étude de femmes sont consommatrices de méthanol, ce qui est Notre étude a connu certaines limites, à savoir, la semblable à l’étude de Sanaei-Zadeh (16). non-réalisation des prélèvements biologiques pour Les signes cliniques et la consommation d’alcool à l’ensemble des patients, d’où la non-collecte des données brûler suggèrent une intoxication au méthanol. Cela a en relation avec la dose de méthanol dans le sang, et la été confirmé lors de l’analyse des lots d’alcool frelaté. non-collecte des données sur la quantité d’alcool ingérée. La répartition des cas par moment d’apparition des symptômes suggère une source commune ponctuelle d’intoxication. En effet, lors de l’enquête, le lot de Conclusion méthanol incriminé a été celui du 19 mai. Le cas index L’enquête a révélé une intoxication collective au a été un consommateur du 20 mai. Ce dernier avait méthanol. Une sensibilisation du grand public au danger présenté une douleur abdominale vers 20 heures, pour du méthanol est importante. Une sensibilisation des laquelle il a été traité. Le 21 mai, à 2 h 30, il est retourné à professionnels de santé aux signes cliniques et à la l’hôpital pour aggravation de cas, où il décède. La létalité conduite à tenir face à une intoxication au méthanol de 65 % dans notre série est proche des valeurs observées s’avère nécessaire. dans la littérature qui oscillent entre 76 % et 89 % (2,3). La littérature montre que, lors de l’ingestion de méthanol, Financement : aucun. l’intoxication passe par plusieurs phases : la phase de Conflits d'intérêts : aucun déclaré.

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Epidemiological profile of methanol poisoning, El Hajeb, Morocco

Abstract Background: Methanol poisoning is of particular importance in low and middle-income countries. We reported on a methanol poisoning incident that occurred 22 May 2017, in El Hajeb (Morocco). Aims: This study aimed to describe the extent of the intoxication, determine its source and implement the necessary preventative measures. Methods: We conducted a cross-sectional survey. A standardized questionnaire including socio-economic data, clinical symptoms and time of use was administered face-to-face to cases of methanol poisoning. Biological samples were taken for toxicological analysis. Data were entered and analyzed on Epi Info version 7. Results: Twenty-six cases of methanol poisoning were surveyed with a mean age of 39.7 (SD 11.1) years and a male/female sex ratio of 5.5. All intoxicated cases were of low socioeconomic status. The mean latency period between use and symp- tom onset was 1.5 (SD 1) days. Reported symptoms were mildly altered consciousness in 14 cases (53.8%), abdominal pain in 10 cases (38.5%), headache in 9 cases (34.6%), vomiting in 8 cases (30.8%) and coma in 7 cases (27.1%). Mortality was 65% and 4 cases developed blindness. Laboratory results confirmed the presence of methanol in the blood with values greater than 0.6 g/L. The dose of methanol in the associated bottle was 217 g/L. Conclusion: Public awareness of the dangers of methanol intoxication is important. Health professionals need to be aware of the clinical signs and what to do in the event of methanol poisoning.

املرتسم الوبائي للتسمم بامليثانول، مدينة احلاجب، املغرب سنا الصايغ، مريمة بحالو، مريم الصايغ، تورية الصايغ اخلالصة اخللفية: يمثل التسمم بامليثانول ًمشكلة خاصة يف البلدان املنخفضة واملتوسطة الدخل. وقد أبلغنا عن حالة تسمم بامليثانول حدثت بتاريخ 22 مايو/ أيار 2017 يف مدينة احلاجب املغربية. األهداف: هدفت هذه الدراسة إىل وصف درجة التسمم، وحتديد مصدره، وتنفيذ التدابري الوقائية الالزمة. طرق البحث: أجرينا ًمسحا ً.مقطعيا كام أجرينا ًاستبيانا ًوجهالوجه مع حاالت تسمم بامليثانول واشتمل عىل البيانات االجتامعية واالقتصادية، Epi-Info-version واألعراض الرسيرية، ووقت تناول الكحول. ُوجعت عينات بيولوجية لتحليل السمية هبا. واستخدمنا برنامج (7) إلدخال البيانات وحتليلها. النتائج: شمل املسح 26 حالة تسمم بامليثانول، وبلغ متوسط أعامر احلاالت 39.7 ً عاما)االنحراف املعياري 11.1(. وبلغت نسبة الذكور إىل اإلناث 5.5. وكانت جيع حاالت التسمم ذات وضع اجتامعي واقتصادي منخفض. وبلغ متوسط فرتة الكمون بني تعاطي الكحول وبداية األعراض 1.5 ًيوما )االنحراف املعياري (.1 وكانت أكثر األعراض ُاملبلغ عنها هي: تغري خفيف يف الوعي يف 14 حالة )53.8%(، وآالم يف البطن يف 10 حاالت )38.5%(، وصداع يف 9 حاالت )34.6%(، وقيء يف 8 حاالت )30.8%(، وغيبوبة يف 7حاالت )27.1%(. وبلغ معدل اإلماتة % 65من احلاالت، كام أصيبت 4 حاالت بالعمى. وأكدت النتائج املختربية وجود ميثانول يف الدم بكميات تزيد عن 0.6 جرام/لرت. وبلغت جرعة امليثانول يف القارورة التي تسببت يف الرضر 217جرام/لرت. االستنتاجات: مناملهم زيادة الوعي العام بأخطار التسمم بامليثانول. وجيب توعية املهنيني الصحيني بالعالمات الرسيرية، وباإلجراءات الواجب اختاذها يف حالة التسمم بامليثانول.

Références 1. Methanol. Properties, production, uses, & poisoning. Encyclopaedia Britannica (s.d). (https://www.britannica.com/science/ methanol, consulté le 20 mars 2020). 2. Zobnine IV, Liubimov BM, Malyh AF,TretyakovAB, Teterina IP, Pazukov EA, et al. Intoxication collective par le méthanol à Irkoutsk en décembre 2016. Toxicol Anal Clin. 2017 May;29(2S):S77–S78. https://doi.org/10.1016/j.toxac.2017.03.118 3. Liu JJ, Daya MR, Carrasquillo O, Kales NS. Prognostic factors in patients with methanol poisoning. J Toxico Clin Toxicol. 1998;36(3):175–81. https://doi.org/10.3109/15563659809028937

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4. Jacobsen D, Jansen H, Wiik‐Larsen E, Bredesen JE, Halvorsen S. Studies on methanol poisoning, Acta Med Scand. 1982;212(1- 2):5–10. https://doi.org/10.1111/j.0954-6820.1982.tb03160.x 5. Palatnick W, Redman LW, Sitar DS, Tenenbein M. Methanol half-life during ethanol administration: implications for management of methanol poisoning. Ann Emerg Med. 1995 Aug;26(2):202–7. https://doi.org/10.1016/S0196-0644(95)70152-4 6. McCoy HG, Cipolle RJ, Ehlers SM, Sawchuk RJ, Zaske DE. Severe methanol poisoning: application of a pharmacokinetic model for ethanol therapy and hemodialysis. Am J Med. 1979 Nov;67(5):804–7. https://doi.org/10.1016/0002-9343(79)90738-1 7. Recensement général de la population et de l’habitat 2014 : Population légale du Maroc. Rabat: Haut-Commissariat au Plan; 2018 (https://www.hcp.ma/downloads/RGPH-2014_t17441.html, consulté le 23 mars 2020). 8. Rhalem N, Jalal G, Soulaymani R. Intoxication par le méthanol. 1996 (https://docplayer.fr/27698320-Intoxication-par-le- methanol-n-rhalem-gh-jalal-r-soulaymani.html). 9. Sutton TL, Foster RL, Liner SR. Acute methanol ingestion. Pediatr Emerg Care. 2002 Oct;18(5):360–3. https://doi. org/10.1097/00006565-200210000-00009 10. Jacobsen D, McMartin KE. Methanol and ethylene glycol poisonings. Mechanism of toxicity,clinical course, diagnosis and treatment. Med Toxicol. 1986 Sep-Oct;1(5):309–34. https://doi.org/10.1007/bf03259846 11. Treichel JL, Henry MM, Skumatz CM, Eells JT, Burke JM. Formate, the toxic metabolite of methanol, in cultured ocular cells. Neurotoxicology. 2003 Dec;24(6):825–34. https://doi.org/10.1016/S0161-813X(03)00059-7 12. Kurtas O, Imre KY, Ozer E, Can M, Birincioglu I, Butun C, et al. The evaluation of deaths due to methyl alcohol intoxication. Biomed Res. 2017;28(8):3680–7. 13. Théfenne H, Turc J, Carmoi T, Gardet V, Renard C. Intoxication aiguë au méthanol : réfexion à partir d’un cas. Ann Biol Clin. 2005;63(5):556–60. (https://docplayer.fr/57683568-Abc-intoxication-aigue-au-methanol-refexion-a-partir-d-un-cas-pratique- quotidienne.html). 14. United Nations Environment Programme (UNEP)/International Labour Organization (ILO)/World Health Organization (WHO). International Programme on Chemical Safety (IPCS). Methanol. Geneva: World Health Organization; 1997 (Environmental Health Criteria Series, No 196). 15. Paasma R, Hovda KE, Tikkerberi A, Jacobsen D. Methanol mass poisoning in Estonia: outbreak in 154 patients. Clin Toxicol(Phila). 2007;45(2):152–7. https://doi.org/10.1080/15563650600956329. 16. H. Sanaei-Zadeh H, S.K. Esfeh SK, N. Zamani N, F. Jamshidi F, S. Shadnia S. Hyperglycemia is a strong prognostic factor of lethality in methanol poisoning, J Med Toxicol. 2011 Sep;7(3):189–4. https://doi.org/10.1007/s13181-011-0142-x. 17. Francis ST, Nair JR, Shiji PV, Mohamed S, Geetha P, Sasidharan PK. A case series of acute methanol poisoning from Northern Kerala. Emergency Med. 2016;6(2): 312. https://doi.org/10.4172/2165-7548.1000312.

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Enteric and diarrhoeal diseases surveillance, prevention and control in the Eastern Mediterranean Region1

Citation: Enteric and diarrhoeal diseases surveillance, prevention and control in the Eastern Mediterranean Region. East Mediterr Health J. 2019;26(11):1430–1431. https://doi.org/10.26719/2020.26.11.1430 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 · share experiences from countries on the use of typhoid conjugate vaccine, including for prevention Estimates suggest that the incidence of diarrhoeal dis- and control of extensively drug-resistant salmonella eases in 2015 in the WHO Eastern Mediterranean Region typhoid (XDR S. Typhi); and exceeded 300 million episodes, with children under five years of age accounting for 53% of cases (1). Over 103 692 · develop an overall approach for the prevention and deaths from diarrhoea occurred in the Region in 2015, control of diarrhoeal diseases in the Region. with a mortality rate of 16.0 per 100 000 (1). The majority of these deaths (63.3%) occurred in children aged un- Summary of discussions der 5 years (65 670 deaths); WHO estimates that in 2017 there were 11–21 million cases of typhoid fever, leading to Discussions demonstrated the interest of countries in 128 000–161 000 deaths (1). improving their surveillance systems for diarrhoeal diseases, based on other countries’ experience. Improv- Adopting parallel approaches to managing the ing rotavirus vaccine coverage was seen as crucial for separate agents of diarrhoeal diseases does not constitute decreasing diarrhoeal disease morbidity and mortality an efficient approach to prevention and control. Within among children under 5 years of age. It was also agreed the WHO Regional Office for the Eastern Mediterranean, that surveillance, outbreak preparedness and response, the Vaccine Preventable Diseases/Polio Transition coupled with WASH preventive measures, need to be unit of the Department of Universal Health Coverage/ combined to manage and control cholera outbreaks in the Communicable Diseases and the Infectious Hazard Region. Participants proposed recommendations based Management unit of the WHO Health Emergencies on the knowledge and experiences shared by countries programme have initiated an integrated approach to and the support offered by partners. The recommenda- addressing diarrhoeal diseases under one programme tions point to the need for robust integrated approaches that encompasses all interventions. As part of this to all aspects of surveillance, prevention and control of initiative, the WHO Regional Office held a meeting diarrhoeal diseases in the Region. The recommendations in Cairo, Egypt, from 2 to 5 March 2020 on enteric and addressed several areas including surveillance, outbreak diarrhoeal diseases surveillance, prevention and control preparedness and response, case management, laborato- with a focus on cholera, typhoid and rotavirus in the ry enhancement, and building on existing systems and 2 Eastern Mediterranean Region ( ). mechanisms to optimize health benefits and make use of The objectives of the meeting were to: existing resources. · understand the epidemiology and overall burden of diarrhoeal diseases, including rotavirus, cholera and Recommendations typhoid fever, in the Eastern Mediterranean Region; · share lessons learned from global paediatric diarrhoe- To WHO al surveillance and rotavirus surveillance progress in · Surveying countries in the Region to assess diarrhoe- relation to rotavirus vaccine introduction; al disease surveillance capacity and data needs, in or- · share global updates on the rotavirus vaccine availa- der to guide WHO and partners on the establishment ble and in the pipeline; of a comprehensive diarrhoeal diseases surveillance system; · discuss the current cholera and typhoid situation in the Region and challenges to managing current out- · establishing rotavirus surveillance in countries where breaks, including cross-border coordination mecha- it does not exist; nisms; · establishing a rotavirus regional reference laboratory; · share experiences from countries on the use of oral · enhancing capacities in the Region to track XDR-ty- cholera vaccine, including in prevention and control phoid in coordination with work on antimicrobial of cholera in the Region; resistance in S. Typhi;

1 This summary is extracted from the Summary report on the Meeting on enteric and diarrhoeal diseases surveillance, prevention and control with a focus on cholera, typhoid and rotavirus in the Eastern Mediterranean Region, Cairo, Egypt, 2–5 March 2020 (https://applications.emro.who.int/docs/ WHOEMEPI359E-eng.pdf?ua=1).

1430 WHO events addressing public health priorities EMHJ – Vol. 26 No. 11 – 2020

· improving understanding of the burden of typhoid To Member States fever in countries of the Region and increase aware- · Strengthening capacity to follow diagnostic proce- ness and advocacy for the prevention and control of dures and case management of typhoid and cholera typhoid fever (and associated antimicrobial resist- as per WHO recommendations; ance) as a public health priority in the Region; · adopting a multisectoral approach, including collab- · developing or updating national cholera control plans oration between different ministries, in prevention aligned to the Ending Cholera global 2030 roadmap; and control of cholera outbreaks; and · aligning the national cholera control plan to the End- · coordinating with relevant institutions to conduct ing Cholera global roadmap; and modelling and forecasting studies for cholera and other waterborne diseases. · enhancing community awareness and engagement, as an integral component of prevention and control of diarrhoeal diseases.

References 1. World Health Organization. Immunization, vaccines and biologicals – typhoid. Geneva: World Health Organization; 2019 (https://www.who.int/immunization/diseases/typhoid/en/). 2. World Health Organization Regional Office for the Eastern Mediterranean (WHO/EMRO). Meeting on enteric and diarrhoeal diseases surveillance, prevention and control with a focus on cholera, typhoid and rotavirus in the Eastern Mediterranean Region, Cairo, Egypt, 2–5 March 2020. Cairo: WHO/EMRO; 2020 (https://applications.emro.who.int/docs/WHOEMEPI359E-eng. pdf?ua=1).

1431 Eastern Mediterranean Health Journal Members of the WHO Regional Committee for the Eastern Mediterranean IS the official health journal published by the Eastern Mediterranean Regional Office of the World Health Organization. It is a forum for Afghanistan . Bahrain . Djibouti . Egypt . Islamic Republic of Iran . Iraq . Jordan . Kuwait . Lebanon the presentation and promotion of new policies and initiatives in public health and health services; and for the exchange of ideas, concepts, Libya . Morocco . Oman . Pakistan . Palestine . Qatar . Saudi Arabia . Somalia . Sudan . Syrian Arab Republic epidemiological data, research findings and other information, with special reference to the Eastern Mediterranean Region. It addresses Tunisia . United Arab Emirates . Yemen all members of the health profession, medical and other health educational institutes, interested NGOs, WHO Collaborating Centres and individuals within and outside the Region. البلدان أعضاء اللجنة اإلقليمية ملنظمة الصحة العاملية لرشق املتوسط املجلة الصحية لرشق املتوسط األردن . أفغانستان . اإلمارات العربية املتحدة . باكستان . البحرين . تونس . ليبيا . مجهورية إيران اإلسالمية هىاملجلة الرسمية التى تصدر عن املكتب اإلقليمى لرشق املتوسط بمنظمة الصحة العاملية. وهى منرب لتقديم السياسات واملبادرات اجلديدة يف الصحة العامة ...... اجلمهورية العربية السورية جيبويت السودان الصومال العراق عُ ام ن فلسطني قطر الكويت لبنان مرص املغرب واخلدمات الصحية والرتويج هلا، ولتبادل اآلراء واملفاهيم واملعطيات الوبائية ونتائج األبحاث وغري ذلك من املعلومات، وخاصة ما يتعلق منها بإقليم رشق اململكة العربية السعودية . اليمن املتوسط. وهى موجهة إىل كل أعضاء املهن الصحية، والكليات الطبية وسائر املعاهد التعليمية، وكذا املنظامت غري احلكومية املعنية، واملراكز املتعاونة مع منظمة الصحة العاملية واألفراد املهتمني بالصحة ىف اإلقليم وخارجه. Membres du Comité régional de l’OMS pour la Méditerranée orientale La Revue de Santé de la Méditerranée Orientale Afghanistan . Arabie saoudite . Bahreïn . Djibouti . Égypte . Émirats arabes unis . République islamique d’Iran EST une revue de santé officielle publiée par le Bureau régional de l’Organisation mondiale de la Santé pour la Méditerranée orientale. Elle Iraq . Libye . Jordanie . Koweït . Liban . Maroc . Oman . Pakistan . Palestine . Qatar . République arabe syrienne offre une tribune pour la présentation et la promotion de nouvelles politiques et initiatives dans le domaine de la santé publique et des Somalie . Soudan . Tunisie . Yémen services de santé ainsi qu’à l’échange d’idées, de concepts, de données épidémiologiques, de résultats de recherches et d’autres informations, se rapportant plus particulièrement à la Région de la Méditerranée orientale. Elle s’adresse à tous les professionnels de la santé, aux membres des instituts médicaux et autres instituts de formation médico-sanitaire, aux ONG, Centres collaborateurs de l’OMS et personnes concernés au sein et hors de la Région.

EMHJ is a trilingual, peer reviewed, open access journal and the full contents are freely available at its website: http://www/emro.who.int/emhj.htm

EMHJ information for authors is available at its website: http://www.emro.who.int/emh-journal/authors/

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