Contents

Editorial

Moving away from the comfort zone of tobacco control policies to the highest level of implementation...... 161 Research articles

Risk factors for neonatal intensive care unit admission in Amman, Jordan...... 163 Trend of bacterial meningitis in Bahrain from 1990 to 2013 and effect of introduction of new vaccines...... 175 Change in attitudes and knowledge of problem drug use and harm reduction among a Eastern Mediterranean community cohort in Kabul, Afghanistan...... 183 Accuracy of the VITEK® 2 system for a rapid and direct identification and susceptibility testing Health Journal of Gram-negative rods and Gram-positive cocci in blood samples...... 193 Review Routine immunization services in Pakistan: seeing beyond the numbers...... 201 La Revue de Santé de Volume 22 Number 3 Short communications la Méditerranée orientale Responding to physical and psychological health impacts of disasters: case study of the Iranian disaster rehabilitation plan...... 212 Environmental carcinogen exposure and lifestyle factors affecting cancer risk in Qatar:

findings from a qualitative review...... 219 March 2016 Letter to the Editor

Medical error reporting: is it about physicians’ knowledge and their practice, or patient safety culture in the workplace?...... 228

WHO events addressing public health priorities

Implementing the WHO FCTC: the need to scale up tobacco control...... 230

Effective and affordable tobacco control policies and measures are well established, including banning smoking in all public places and taxing tobacco products. Countries of the Region need to step up their implementation of tobacco control measures in order to make greater progress towards achieving the targeted 30% reduction in tobacco use by 2025.

املجلد الثاين والعرشون / عدد Volume 22 / No. 3 3 مارس/آذار March/Mars 2016

Cover 22-03.indd 154-156 6/9/2016 1:15:29 PM Members of the WHO Regional Committee for the Eastern Mediterranean املجلة الصحية لرشق املتوسط Afghanistan . Bahrain . Djibouti . Egypt . Islamic Republic of Iran . Iraq . Jordan . Kuwait . Lebanon هى املجلة الرسمية التى تصدر عن املكتب اإلقليمى لرشق املتوسط بمنظمة الصحة العاملية. وهى منرب لتقديم السياسات Libya . Morocco . Oman . Pakistan . Palestine . Qatar . Saudi Arabia . Somalia . Sudan . Syrian Arab واملبادرات اجلديدة ىف اخلدمات الصحية والرتويج هلا، ولتبادل اآلراء واملفاهيم واملعطيات الوبائية ونتائج األبحاث وغري Republic . Tunisia . United Arab Emirates . Yemen ذلك من املعلومات، وخاصة ما يتعلق منها بإقليم رشق 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.

EASTERN MEDITERRANEAN HEALTH JOURNAL البلدان أعضاء اللجنة اإلقليمية ملنظمة الصحة العاملية لرشق املتوسط IS the official health journal published by the Eastern Mediterranean Regional Office of the World Health Organization. It is a forum for the presentation and promotion of new policies and initiatives in health services; and for the exchange of ideas, con‑ األردن . أفغانستان . اإلمارات العربية املتحدة . باكستان . البحرين . تونس . ليبيا . مجهورية إيران اإلسالمية .cepts, epidemiological data, research findings and other information, with special reference to the Eastern Mediterranean Region اجلمهورية العربية السورية . اليمن . جيبويت . السودان . الصومال . العراق . عُ ام ن . فلسطني . قطر . الكويت . لبنان . مرص ‑It addresses all members of the health profession, medical and other health educational institutes, interested NGOs, WHO Col laborating Centres and individuals within and outside the Region. املغرب . اململكة العربية السعودية LA REVUE DE SANTÉ DE LA MÉDITERRANÉE ORIENTALE EST une revue de santé officielle publiée par le Bureau régional de l’Organisation mondiale de la Santé pour la Méditerranée orientale. Elle offre une tribune pour la présentation et la promotion de nouvelles politiques et initiatives dans le domaine des ser‑vices de santé ainsi qu’à l’échange d’idées, de concepts, de données épidémiologiques, de résultats de recherches et d’autres Membres du Comité régional de l’OMS pour la Méditerranée orientale 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 collabora‑ Afghanistan . Arabie saoudite . Bahreïn . Djibouti . Égypte . Émirats arabes unis . République islamique d’Iran teurs de l’OMS et personnes concernés au sein et hors de la Région. Iraq . Libye . Jordanie . Koweït . Liban . Maroc . Oman . Pakistan . Palestine . Qatar . République arabe syrienne Somalie . Soudan . Tunisie . Yémen

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/

EMHJ is abstracted/indexed in the Index Medicus and MEDLINE (Medical Literature Analysis and Retrieval Systems on Line), ISI Web of knowledge, the Cumulative Index to Nursing and Allied Health Literature (CINAHL), Embase, Lexis Nexis, Scopus and the Index Medicus for the WHO Eastern Mediterranean Region (IMEMR). Correspondence

Editor-in-chief Eastern Mediterranean Health Journal ©World Health Organization 2016 WHO Regional Office for the Eastern Mediterranean All rights reserved P.O. Box 7608 Nasr City, Cairo 11371 Disclaimer Egypt The designations employed and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of the World Health Organization concerning the legal status of any country, territory, city or area or of Tel: (+202) 2276 5000 its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted lines on maps represent approximate border Fax: (+202) 2670 2492/(+202) 2670 2494 lines for which there may not yet be full agreement. The mention of specific companies or of certain manufacturers’ products Email: [email protected] does not imply that they are endorsed or recommended by the World Health Organization in preference to others of a similar nature that are not mentioned. All reasonable precautions have been taken by the World Health Organization to verify the information contained in this publication. However, the published material is being distributed without warranty of any kind, either express or implied. The responsibility for the interpretation and use of the material lies with the reader. In no event shall the World Health Organization be liable for damages arising from its use. The named authors alone are responsible for the views expressed in this publication. Subscriptions and Permissions Publications of the World Health Organization can be obtained from Knowledge Sharing and Production, World Health Organization, Regional Office for the Eastern Mediterranean, ISSN 1020-3397 PO Box 7608, Nasr City, Cairo 11371, Egypt (tel: +202 2670 2535, fax: +202 2670 2492; email: [email protected]). Requests for permission to reproduce, in part or in whole, or to translate publications of WHO Regional Office for the Eastern Mediterranean – whether for Cover designed by Diana Tawadros sale or for noncommercial distribution – should be addressed to WHO Regional Office for Internal layout designed by Emad Marji and Diana Tawadros the Eastern Mediterranean, at the above address; email: [email protected]. Printed by WHO Regional Office for the Eastern Mediterranean Cover photograph ©World Health Organization

Cover 22-03.indd 157-159 6/9/2016 1:15:29 PM Eastern Mediterranean La Revue de Santé de Health Journal la Méditerranée orientale

املجلد الثاين و العرشون عدد Vol. 22 No. 3 • 2016 • 3 Contents

Editorial Moving away from the comfort zone of tobacco control policies to the highest level of implementation Fatimah El-Awa, Prasad Vinayak and Douglas Bettcher...... 161 Research articles Risk factors for neonatal intensive care unit admission in Amman, Jordan C.E. Quinn, P. Sivasubramaniam, M. Blevins, A. Al Hajajra, A. Taleb Znait, N. Khuri-Bulos, S. Faouri and N. Halasa...... 163 Trend of bacterial meningitis in Bahrain from 1990 to 2013 and effect of introduction of new vaccines N. Saeed, H. AlAnsari, S. AlKhawaja, J.S. Jawad, K. Nasser and E. AlYousef...... 175 Change in attitudes and knowledge of problem drug use and harm reduction among a community cohort in Kabul, Afghanistan C.S. Todd, M.R. Stanekzai, A. Nasir, K. Fiekert, M.G. Orr, S.A. Strathdee and D. Vlahov...... 183 Accuracy of the VITEK® 2 system for a rapid and direct identification and susceptibility testing of Gram-negative rods and Gram-positive cocci in blood samples N.A. Nimer, R.J. Al-Saa’da and O. Abuelaish...... 193 Review Routine immunization services in Pakistan: seeing beyond the numbers S. Husain and S.B. Omer...... 201 Short communications Responding to physical and psychological health impacts of disasters: case study of the Iranian disaster rehabilitation plan A. Ardalan, S. Sohrabizadeh, M.F. Latifi, M.H. Rajaei, A. Asadi, S. Mirbeigi, N. Rouhi and H. Yousefi...... 212 Environmental carcinogen exposure and lifestyle factors affecting cancer risk in Qatar: findings from a qualitative review R. Denholm, J. Schüz, K. Straif, F.M.H. Ali, F. Bonas, O. Gjebrea, C. Sifton and A.C. Olsson...... 219 Letter to the Editor Medical error reporting: is it about physicians’ knowledge and their practice, or patient safety culture in the workplace?...... 228 WHO events addressing public health priorities Implementing the WHO FCTC: the need to scale up tobacco control...... 230

Book 22-03.indb 159 6/14/2016 8:59:57 AM Ala Alwan, Editor-in-chief Editorial Board Zulfiqar Bhutta Mahmoud Fahmy Fathalla Rita Giacaman Ahmed Mandil Ziad Memish Arash Rashidian Sameen Siddiqi Huda Zurayk International Advisory Panel Mansour M. Al-Nozha Fereidoun Azizi Rafik Boukhris Majid Ezzati Zuhair Hallaj Hans V. Hogerzeil Mohamed A. Ghoneim Alan Lopez Hossein Malekafzali El- Mahgoub Hooman Momen Sania Nishtar Hikmat Shaarbaf Salman Rawaf Editors Fiona Curlet Guy Penet (French) Alison Bichard, Marie-France Roux (Freelance) Manar Abdel-Rahman, Ahmed Bahnassy, Abbas Rahimiforoushani (Statistics) Graphics Suhaib Al Asbahi, Diana Tawadros Administration Nadia Abu-Saleh, Yasmeen Sedky, Iman Fawzy

Book 22-03.indb 160 6/14/2016 8:59:58 AM املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد الثالث

Editorial Moving away from the comfort zone of tobacco control policies to the highest level of implementation Fatimah El-Awa,1 Prasad Vinayak 2 and Douglas Bettcher 3

The year 2015 marked the 10th anniver- second-hand smoke, i.e. a comprehensive prevent and control NCDs. Furthermore, sary of the entry into force of the WHO ban of smoking in all public places (Leba- these measures are very affordable for all Framework Convention on Tobacco non, Libya, Islamic Republic of Iran, Pa- economic groups of countries (6). This Control (FCTC). Following this, in kistan, Palestine and Saudi Arabia), and recipe has been implemented nearly in the same year, the 18th comprehensive only six have completely banned tobacco full in only one country in the Region, the national tobacco control law(s) was advertising promotion and sponsorship Islamic Republic of Iran and, as expected, adopted in the WHO Eastern Mediter- (Bahrain, Djibouti, Islamic Republic of the country has been able to reduce the ranean Region (EMR) (1). Iran, Libya, United Arab Emirates and prevalence of tobacco use. According to Member countries of the EMR have Yemen). Although 12 countries are the WHO trend report of 2015, the Is- come a long way in tobacco control leg- implementing graphic health warnings lamic Republic of Iran is the one country islation since the entry into force of the (Bahrain, Djibouti, Egypt, Islamic Re- in the Region that will witness a reduction WHO FCTC, with 19 of the 22 countries public of Iran, Jordan, Kuwait, Oman, Pa- in tobacco use by the year 2025, although, now party to it (except Morocco, Pales- kistan, Qatar, Saudi Arabia, United Arab due to the lack of a good taxation policy, it tine and Somalia). But has this legal move- Emirates and Yemen), only three of them won’t be able to achieve the target level of have achieved the highest level in the reduction in tobacco use ( ). ment really succeeded in changing the 7 policy (Djibouti, Egypt and Islamic Re- prevalence of tobacco use in the Region? Looking at the key demand reduc- public of Iran). As regards taxation, only tion measures in the MPOWER and The recent tobacco trends report, Jordan and Palestine have implemented NCD tobacco control best buys, as in- published by WHO in 2015 (2), clearly a total tax of at least 75% of the retail price dicated in the 2015 WHO Report on indicates that none of the WHO regions of cigarettes (data collection does not the Global Tobacco Epidemic (8), there will achieve the targeted 30% reduction cover any other tobacco products) (4). are two features clearly common among in tobacco use by 2025 (3). Even worse, The small number of countries achieving the majority of EMR countries. First, two regions are on the contrary expected the highest level in the various tobacco most of the countries have only made to witness an increase in tobacco use: the control policies has thus resulted in only moderate progress because implemen- African region and the EMR. In 2015, the modest success in reducing tobacco use tation of tobacco control policies has prevalence of tobacco use in the EMR throughout the Region. been at a middle level of achievement, was 21.0% and by 2025 it is projected Tobacco use is a risk factor that could neither the highest nor the lowest, in to be 24.5%. The estimated 90 million impede achievement of the target of a other words a “comfort zone” level. Thus, smokers in the Region in 2015 could 25% reduction in mortality from NCDs some improvement is happening but this grow to 129 million in just 10 years. (cardiovascular diseases, cancer, diabetes is not sufficient to achieve a reduction The wave of legislation adoption in or chronic respiratory disease) by 2025. in the prevalence at the rate agreed by the Region has not reduced tobacco use However, the recipe for successfully con- the countries when adopting the NCD in the majority of the countries for many trolling this risk factor is not a mystery. Global Action Plan in 2013. The fact that reasons, most importantly because the Effective tobacco control policies have many countries prefer this comfort zone legislation and policies for the key de- been well known since the adoption of to fighting to achieve the highest level of mand reduction measures have not been the WHO FCTC in 2003, and follow- the policy has two serious impacts. First, adopted at the highest level of achieve- ing WHO’s launch of a set of measures it exhausts the legislative system and un- ment. Only six countries have achieved (MPOWER) in 2008 (5) are recog- dermines chances for further legislative the highest level of protection from nized as part of the best buy measures to change, blocking the way for real change

1Regional Adviser, Tobacco Free Initiative, World Health Organization Regional Office for the Eastern Mediterranean, Cairo Egypt. 2Manager, Tobacco Free Initiative, World Health Organization, Geneva, Switzerland. 3Director, Department for Prevention of Noncommunicable Diseases, World Health Organization, Geneva, Switzerland. We acknowledge the efforts of Anne-Marie Perucic, Luminita Sanda and Alison Commar for their editorial input and for double checking the figures presented.

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in the future. In addition, it confuses the in reducing the policy level. This incon- in selected countries of the EMR has public on what the real goal of tobacco sistency causes significant difficulty, not shown that if all MPOWER measures are control is. For example, is it to have desig- only in monitoring the impact of the implemented at the highest level, a reduc- nated smoking areas in key public places policies over time, but also by confusing tion in tobacco use prevalence ranging and ensure the public abides by this, or the results at the national level. from 20% to 35% is likely to occur within is it a total ban of tobacco use and hence A further issue is that many countries 5 years (10). Leadership and political no designated smoking areas at all, as per of the Region are experiencing emer- commitment at the national level, seri- the WHO FCTC. In addition, stopping gencies and crises which tend to divert ous legislative change, endorsement of a short of the highest level of achievement attention from tobacco control. These cir- multisectorial approach, and a national in the policy allows the tobacco industry cumstances provide the tobacco industry partnership based on full technical under- to manipulate even these modest targets with the opening to promote its products standing and commitment are indeed the so they become less effective than the and undermine any tobacco control op- way forward. This must be combined with government intended. Thus instead of portunities in these countries (9). implementation of the Article 5.3 guide- achieving the modest level of the policy, Given the situation outlined above, lines of the WHO FCTC on “Protection countries actually achieve even less. Fur- the main concern is that countries will of public health policies with respect to thermore, whilst working to water down need to report on their success in to- tobacco control from commercial and tobacco control efforts and push for non- bacco control on two dates, the NCD other vested interests of the tobacco effective measures, the tobacco industry target date of 2025 and the Sustainable industry” (11). Limiting, if not eliminat- can then twist logic and argue that such Development Goals’ date of 2030. For ing, tobacco industry interference and tobacco control measures are not needed the countries of the Region to succeed influence in decision making processes since they do not work. and achieve the targets set by then, a real is imperative to achieving any progress The second feature that marks the paradigm shift in tobacco control must for tobacco control in the Region.n it will tobacco control movement in the Re- be considered with a greater readiness provide, our ability to respond effectively gion is the game of musical chairs in to fight for the highest level of tobacco to the virus remains uncertain. policy adoption. There is no stability in control best buys. The global fight against the virus will the level of policy achieved; one year Fully implementing the WHO only be a decisive success if a sustained country X might be at the highest policy FCTC and achieving the highest level global response is launched; WHO is level of achievement, but the following in all MPOWER and NCD best buys committed to working with all stake- year changes are introduced that result is a must for moving forward. Research holders to achieve this.

References

1. World Health Organization Regional Office for the Eastern nmh/publications/best_buys_summary.pdf, accessed 1 March Mediterranean. Tobacco Free Initiative. Country legislation 2016). [web page] (http://www.emro.who.int/tobacco/legislation/ 7. WHO global report on trends in prevalence of tobacco smoking, country-legislation.html, accessed 1 March 2016). 2015, Geneva: World Health Organization; 2015 (http://apps. 2. WHO global report on trends in prevalence of tobacco smoking who.int/iris/bitstream/10665/156262/1/9789241564922_eng. 2015. Geneva: World Health Organization; 2015 (http://apps. pdf, accessed 1 March 2016). who.int/iris/bitstream/10665/156262/1/9789241564922_eng. 8. WHO report on the global tobacco epidemic, 2015: raising taxes pdf, accessed 1 March 2016). on tobacco. Regional summary, Appendix 1. Geneva: World 3. World Health Organization. WHO discussion paper: a com- Health Organization; 2015. (http://www.who.int/tobacco/glob- prehensive global monitoring framework and voluntary global al_report/2015/appendix1.pdf?ua=1, accessed 1 March 2016) targets for the prevention and control of NCDs. April 2012 9. Golden Leaf Tobacco Co. Ltd. Middle East – fastest growing re- (http://www.who.int/nmh/events/2012/discussion_pa- gion for cigarettes [web page] (http://www.goldenleaftobacco. per2_20120322.pdf, accessed 1 March 2016). net/index.php?option=com_content&view=article&id=99:mid 4. WHO report on the global tobacco epidemic, 2015: raising dle-east-fastest-growing-region-for-cigarettes&catid=46:news taxes on tobacco. Geneva: World Health Organization; 2015. &Itemid=74, accessed 1 March 2016). (http://www.who.int/tobacco/global_report/2015/en/, ac- 10. Levy DT, Fouad H, Levy J, Dragomir AD, El Awa F. Application cessed 1 March 2016). of the abridged SimSmoke model to four Eastern Mediter- 5. WHO report on the global tobacco epidemic, 2008: the ranean countries. Tob Control. 2015 Jun 16. pii: tobaccocon- MPOWER package. Geneva: World Health Organization; trol-2015-052334. PMID: 26080365 2008. (http://www.who.int/tobacco/mpower/mpower_re- 11. WHO Framework Convention on Tobacco Control: guidelines port_full_2008.pdf, accessed 1 March 2016) for implementation. Article 5.3; Article 8; Articles 9 and 10; 6. World Economic Forum and World Health Organization. From Article 11; Article 12; Article 13; Article 14 – 2013 edition. Geneva: burden to ‘best buys’: reducing the economic impact of non- World Health Organization; 2013 (http://apps.who.int/iris/ communicable diseases in low- and middle-income countries. bitstream/10665/80510/1/9789241505185_eng.pdf, accessed Geneva: World Economic Forum; 2011 (http://www.who.int/ 1 March 2016).

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Risk factors for neonatal intensive care unit admission in Amman, Jordan C.E. Quinn,1 P. Sivasubramaniam,1 M. Blevins,2,3 A. Al Hajajra,5 A. Taleb Znait,5 N. Khuri-Bulos,5,6 S. Faouri 5 and N. Halasa 2,4,7

عوامل خطر إدخال حديثي الوالدة إىل وحدة العناية املركزة يف ّعمن باألردن كريستني كوين فريتز، بريا سيفاسوبر برمنيوم، مريديث بليفينز، أمحد احلجاجرة، أرشف طالب أزنيط، نجوى خوري بولص، سمري فاعوري، ناتاشا هلسه

اخلالصــة: إن ًفهــا أفضــل لعوامــل خطــر إدخــال حديثــي الــوالدة إىل وحــدة العنايــة املركــزة يمكــن أن يرشــد إىل تدخــات ِّحتســن مــن بقــاء حديثــي الــوالدة عــى قيــد احليــاة. وقــد هدفــت هــذه الدراســة إىل بيــان حالــة جمموعــة مــن حديثــي الــوالدة الذيــن أدخلــوا إىل وحــدة العنايــة 96 املركــزة يف ّ ن عــابــاألردن، ومقارنتهــم مــع حديثــي الــوالدة ُخ ِّرجــوا إىل املنــزل. فتــم تســجيل حديثــي الــوالدة خــال ســاعة يف مستشــفى البشــري ً اســتباقيامــن شــباط/فرباير 2010 حتــى حزيران/يونيــو 2011. ُوجعــت البيانــات الســكانية والرسيريــة لألمهــات وحديثــي الــوالدة. مــن أصــل 5466 حديثــي والدة مســجلني تــم إدخــال 373 (%6.8) إىل وحــدة العنايــة املركــزة. وكان متوســط العمــر احلمــي للرضــع الذيــن 49.5 2.2 36 أدخلــوا إىل وحــدة العنايــة املركــزة ًأســبوعا، ووســطي وزن الوليــد كجــم، ُوولــد % منهــم بعمليــة قيرصيــة غــري انتقائيــة. انخفــاض العمــر احلمــي وانخفــاض وزن الوليــد والــوالدة بعمليــة قيرصيــة والــوالدة يف شــهر أيار/مايــو كانــت عوامــل خطــر ذات داللــة إحصائيــة لإلدخــال إىل وحــدة العنايــة املركــزة. إن عوامــل خطــر إدخــال حديثــي الــوالدة إىل وحــدة العنايــة املركــزة كانــت متمشــية مــع شــعوب أخــرى يف العــامل، غــريأن متوســط العمــر احلمــي ووزن حديثــي الــوالدة كانــا أعــى ممــا مهــا عليــه يف البلــدان املتقدمــة.

ABSTRACT A better understanding of risk factors for neonatal intensive care unit (NICU) admission can inform interventions to improve neonatal survival. This study aimed to describe a population of newborns admitted to a NICU in Amman, Jordan, and compare them with newborns discharged to home. Newborns born within 96 hours at Al-Bashir Hospital were enrolled from February 2010 to June 2011. Demographic and clinical data were collected for mothers and newborns. Of 5466 enrolled neonates, 373 (6.8%) were admitted to the NICU. The median gestational age of NICU infants was 36 weeks, median birth weight was 2.2 kg and 49.5% were delivered by non-elective caesarean section. Lower gestational age, lower birth weight, delivery by caesarean section and birth in the month of May were statistically significant risk factors for NICU admission. Risk factors for NICU admission were consistent with other populations worldwide; however, median gestational age and birth weight were higher than in developed countries.

Facteurs de risque pour l’admission en unité de soins intensifs néonatals à Amman (Jordanie)

RÉSUMÉ Une meilleure compréhension des facteurs de risque pour l’admission en unité de soin intensifs néonatals permet d’orienter les interventions en vue d’améliorer la survie des nouveau-nés. La présente étude avait pour objectif de décrire une population de nouveau-nés admis en unité de soins intensifs néonatals à Amman (Jordanie) et de mener une étude comparative avec des nouveau-nés rentrés à domicile. Les nouveau-nés dont la naissance est survenue dans un laps de temps de 96 heures après leur entrée à l’hôpital Al-Bashir ont participé à l’étude entre février 2010 et juin 2011. Des données démographiques et cliniques ont été collectées pour les mères et les nouveau-nés. Sur 5 466 nouveau-nés, 373 (6,8 %) ont été admis en unité de soins intensifs néonatals. L’âge gestationnel médian des enfants admis dans l’unité était de 36 semaines, le poids médian à la naissance était de 2,2 kg et 49,5 % d’entre eux étaient nés par césarienne non élective. Un âge gestationnel plus bas, un poids à la naissance plus faible, une naissance par césarienne et la naissance au cours du mois de mai constituaient des facteurs de risque statistiquement significatifs pour une admission dans l’unité. Ces facteurs de risque coïncidaient avec ceux d’autres populations dans le monde, mais l’âge gestationnel et le poids à la naissance médians étaient plus élevés que dans les pays développés.

1Undergraduate Medical Education; 2Vanderbilt Institute for Global Health, Nashville, Tennessee, United States of America. 3Department of Biostatistics; 4Department of Paediatrics, Vanderbilt University School of Medicine, Nashville, Tennessee, United States of America (Correspondence to C.E. Quinn: [email protected]). 5Al-Basheer Government Hospital, Amman, Jordan. 6Division of Infectious Disease, Jordan University Hospital, Amman, Jordan. 7Vanderbilt University Medical Centre, Nashville, Tennessee, United States of America. Received: 02/09/14; accepted: 10/12/15

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Introduction period, so that the neonatal fraction of vitamin D levels. If cohort members deaths increased from 38.2% to 40.3% were subsequently admitted for Neonatal intensive care has become a of deaths between 2000 and 2010 (8). respiratory illness, another vitamin cornerstone for treatment of premature Thus, interventions focusing on reduc- D level was drawn at that time (12). infants worldwide. In the United States, ing neonatal death, particularly those Female research assistants approached for example, wide access to advances caused by preterm birth, are crucial to all mothers on the postpartum ward in neonatal care such as surfactant achieving MDG 4. during daytime hours from Sunday therapy and antenatal corticosteroids This trend is similar in Jordan, to Thursday. Verbal consent was ob- has resulted in an increase in survival where the U5MR is 21 per 1000 live tained from mothers to obtain heel- of neonates admitted to NICUs across births (9). During the last two decades pricks for blood from their neonates. the country (1). These technological neonatal morbidity has grown to rep- Over the period 1 February 2010 to advances have led to an average cohort resent a larger proportion of overall 30 June 2011 all neonates born at the that would have likely been considered infant mortality (10), with prematu- hospital within 96 hours were eligible non-viable just a few decades ago. rity as the leading cause of the U5MR for inclusion in the study. However, Neonates weighing under 1500 g have (34%), followed by congenital anoma- the majority of infants were discharged shown a steady increase in survival over lies (21%) and birth asphyxia (12%) within 24 hours unless they were admit- the past decade, and neonates born at (9,11). This calls for a focus on neonatal ted to the NICU. 25 weeks now have a 75% survival rate care to reduce the U5MR and achieve The medical records of neonates (2,3). In addition to improvements in MDG 4. However, neither basic de- from the prospective cohort who were survival among the most premature mographic information nor risk fac- admitted to the NICU were obtained neonates, the United States has seen a tors for admission of infants to NICUs and reviewed retrospectively to collect steady decrease in its overall neonatal in the Middle East, including Jordan, additional data about NICU admission mortality rate (deaths under age 28 days are well-documented in the current and outcomes. per 1000 live births) and the most cur- literature. A better understanding of the Data collection rent estimate is around 4 per 1000 live characteristics of infants requiring care births (4). in the NICU can provide direction for Using a standardized case report ques- Globally, childhood mortality is of interventions that would improve neo- tionnaire, mothers in the prospective particular interest as the world strives to natal survival. Therefore, in this study cohort study were queried in by meet Millennium Development Goal we aimed to describe the demographic a member of the research team, who (MDG) 4: reducing child mortality and clinical characteristics of mothers subsequently recorded the answers by two-thirds between 1990 and 2015 and infants admitted to a NICU and to in English. The research assistants all (5). Currently, 40% of deaths in chil- estimate the risk factors for admission received prior training in the protocol dren younger than 5 years old occur to the NICU of Al Bashir Government for questionnaire administration to in the neonatal period, with 99% of Hospital, one of three major hospitals ensure consistency. Parents were asked neonatal deaths occurring in low- or serving Amman, Jordan. to provide the nationality of the mother middle-income countries (6). This and father, child’s date of birth, route of represents a 30-fold higher average delivery, child’s birth weight, mother’s daily mortality rate during the neonatal Methods vitamin D supplementation history, dai- period than the post-neonatal period ly number of hours that mother spends (7). Complications related to preterm The study was designed as a retrospec- outdoors, mother’s clothing practice, birth accounted for the largest frac- tive cohort nested within a prospective whether or not the mother smoked tion (14.1%) of these deaths, followed cohort study. This study was approved during pregnancy (and if so, which of by intrapartum-related complications by the University of Jordan and the in- the trimesters), and if the mother was (9.4%) and neonatal sepsis or meningi- stitutional review boards of Vanderbilt exposed to smoke in her household tis (5.2%) (8). Though there has been University and the Jordanian Ministry during pregnancy. The questionnaire an overall reduction in the under-5 of Health at Al Bashir Hospital. also asked for self-reported diagnoses mortality rate (U5MR) by an average with medical conditions that may be of 2.6% per year, the decrease falls short Sample associated with decreased bone health, of the 4.4% annual decrease needed to This study was part of a larger neonatal including hyperparathyroidism, gesta- reach MDG 4. Additionally, decreases cohort study that enrolled neonates tional diabetes, rheumatoid arthritis, in U5MR have occurred more rap- born at Al Bashir Government Hos- and diseases requiring corticosteroid idly in children outside of the neonatal pital for baseline assessment of their treatment.

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For the retrospective data collec- Results < 0.001) (Table 1). Neonates of Pal- tion an electronic form was used to estinian nationality were more likely to collect the following variables for every During the 17-month study period, be admitted to the NICU compared neonate admitted to the NICU: reason 19 604 babies were born at Al-Bashir with neonates of other nationalities for admission, Apgar score, C-reactive Hospital: 2810 non-viable (14.3%) and (12% NICU versus 9% non-NICU, P protein measurements, duration of stay 16 794 living neonates. Of the living = 0.018). No differences in vitamin D in the NICU, presence of complica- neonates, 3317 (19.8%) were admitted levels were noted, with a median of 3.5 tions associated with prematurity, early to the NICU. ng/mol in both groups. Certain vitamin and late infection status, antibiotic ad- supplements were more commonly ministration, surfactant administration Characteristics of prospective used during pregnancy by the mothers cohort sample and ventilation strategy. Apgar score of NICU neonates than non-NICU was considered low if it was < 7. Ma- During that same time period, we ap- neonates: a multivitamin, vitamin D, ternal risk factors such as gestational proached 6057 mothers of neonates folic acid, calcium and iron (P < 0.001). diabetes mellitus, premature rupture and enrolled 5466 neonates (90%) in NICU neonates were also more likely of membranes, chorioamnionitis and our prospective cohort (2697 females to be born to a mother that had a higher pre-eclampsia were also recorded when and 2769 males) (Figure 1). The neo- body mass index, history of diabetes, documented in the infant’s chart. All nates in the prospective cohort had a gestational diabetes and pregnancy- data were entered into a secured elec- median gestational age of 39 weeks, induced hypertension than were non- tronic database (Vanderbilt REDCap) median birth weight of 3.1 kg and cae- NICU neonates (P < 0.001, Table 1). (13). sarean section delivery rate of 20% (Ta- Other maternal factors-including age, ble 1). All caesarean sections performed level of education, clothing practice Statistical analysis were non-elective. and location of prenatal care were not Descriptive statistics were used to The mothers in the cohort study had significantly different between the two summarize the sociodemographic and a median age of 27 years and 24% had a groups. clinical characteristics of newborns history of multivitamin use during preg- by NICU admission. A multivariable nancy. The vast majority of women were Multivariable logistic logistic regression model was used to healthy; the two most common medical regression analysis of risk factors for NICU admission estimate the association of maternal conditions reported by mothers were exposure and birth outcomes with rheumatoid arthritis (2%) and gesta- Multivariable logistic regression was NICU admission. Covariates were tional hypertension (2%). Although employed to estimate neonatal and ma- identified a priori, and they included: only 7% of mothers reported smoking ternal factors that were independently baby’s sex, gestational age, birth weight during pregnancy, 72% reported expo- associated with admission to the NICU and type of delivery; mother’s age, sure to tobacco smoke. (Table 2, Figure 2). Lower gestational education, prenatal care, clothing prac- Of the 5466 neonates in the pro- age was associated with NICU admis- tice, hours spent outdoors, exposure spective cohort, 373 (7%) were admit- sion. Compared with a gestational age to tobacco smoke and any vitamin D ted to the NICU during the study of 40 weeks, neonates born at 34 or supplementation; and baby’s date of period (Table 1). Nearly half of these 36 weeks had a higher risk of NICU birth (temporal trend). To account for (183/373) were caesarean section de- admission (OR 8.4; 95% CI: 5.6–12.4 possible non-linear associations, con- liveries, of which 53 (29%) were for fetal and OR 3.6; 95% CI: 2.7–4.8 respec- tinuous variables were included in the indications and 130 (71%) were for tively). Neonates born weighing 2.5 kg models using restricted cubic splines maternal indications. had over 5 times higher odds of NICU (14). Missing values of covariates were admission compared with those with accounted for using multiple imputa- Newborn characteristics by a birth weight of 3 kg (OR 5.39; 95% tion techniques which used predictive NICU admission CI: 4.44–6.55). Delivery by caesarean mean matching to take random draws In the retrospective analysis compar- section had over twice the odds of from imputation models; 25 imputa- ing NICU to non-NICU neonates, NICU admission (OR 2.36; 95% CI: tion data sets were used in the analysis NICU neonates had a lower median 1.71–3.23). Babies born in May 2010 (15). We employed R statistical soft- gestational age (36 weeks versus 39 and May 2011 were also more likely to ware, version 2.15.1 (www.r-project. weeks, P < 0.001); lower median birth be admitted to the NICU (OR 2.43; org) for all data analyses. Analysis weight (2.2 kg versus 3.1 kg, P < 0.001); 95% CI: 1.45–4.10). No significant scripts are available at http://biostat. and were more likely to be delivered by associations were detected between mc.vanderbilt.edu/ArchivedAnalyses. caesarean section (49% versus 18%, P NICU admission and maternal factors

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19604 births during study period

2810 nonviable 16794 living births neonates

6057 mothers approached

5466 neonates 591 mothers declined enrolled participation

373 neonates admitted to the NICU

183 C-sections 190 NSVD

130 maternal 53 fetal Indication Indication

Figure 1 Overview of prospective cohort sample (NICU = neonatal intensive care unit; NSVD = normal spontaneous vaginal delivery)

such as age, education level, location of versus 2.25 kg, P = 0.039) than neonates P < 0.001). Neonates born by caesarean prenatal care or clothing practice. delivered by caesarean section. Addi- section had a higher rate of death in the tionally, compared with vaginal delivery, hospital than neonates born vaginally, NICU patient characteristics caesarean section was associated with but this difference was not significant and outcomes by delivery type the following characteristics: admission (10% versus 7%, P = 0.506). To further characterize differences of for low Apgar score (11% versus 1%, neonates admitted to the NICU, we P < 0.001), use of nasal cannula (44% compared neonates delivered by vaginal versus 30%, P = 0.01), use of surfactant Discussion delivery or caesarean section (Table 3). (12% versus 4%, P = 0.029), lower white Of the 373 NICU neonates, 318 (85%) blood cell count (13.1 versus 13.9 × This is one of the first studies describing had charts available for retrospective 109/L, P = 0.047), more days in the neonates admitted to a NICU in Am- review. Comparing mode of delivery, hospital (4 days versus 3 days, P= 0.002) man, Jordan and estimating the associ- children born by vaginal delivery had a and more days on antibiotics (4 days ated risk factors for NICU admission. In significantly higher median gestational versus 3 days, P = 0.002) (Table 3). our study, we found that neonates admit- age [interquartile range (IQR) 35–37 Maternal diagnosis of pre-eclampsia ted to the NICU had lower birth weight weeks versus 34–37 weeks, P = 0.016] was significantly associated with a cae- and gestational age compared with and higher median birth weight (2.30 kg sarean section delivery (18% versus 2%, neonates not admitted to the NICU.

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Table 1 Newborn characteristics by neonatal intensive care unit (NICU) admission in Amman, Jordan Variable NICU Non-NICU Total P-value (n = 373) (n = 5093) (n = 5466) Sex Female [no. (%)] 165 (44) 2532 (50) 2697 (49) 0.047 Gestational age Gestational age (weeks) [median (IQR)] 36 (34–38) 39 (38–40) 39 (38–40) < 0.001 Age range (weeks) 25–43 24–43 24–43 Birth weight Birth weight (kg) [median (IQR)] 2.2 (1.9–3) 3.1 (2.9–3.5) 3.1 (2.8–3.5) < 0.001 Weight range (kg) 0.5–5.6 1.3–5.0 0.5–5.6 Type of delivery [no. (%)] < 0.001 Normal spontaneous vaginal 190 (51) 4162 (82) 4352 (80) Caesarean section 183 (49) 929 (18) 1112 (20) Mother’s age Age (years) [median (IQR)] 27 (23–33) 27 (22–32) 27 (22–32) 0.154 Mother’s BMI BMI (kg/m2) [median (IQR)] 25.0 (21.6–28.0) 23.6 (21.3–26.6) 23.8 (21.4–26.7) < 0.001 Missing values [no. (%)] 176 (47) 3330 (65) 3506 (64) Mother’s highest education level [no. (%)] 0.347 Primary education 84 (34) 883 (33) 967 (33) Secondary education 130 (52) 1293 (49) 1423 (49) College education 31 (12) 370 (14) 401 (14) No education 4 (2) 92 (3) 96 (3) Missing values 124 (33) 2455 (48) 2579 (47) Mother’s nationality [no. (%)] 0.018 Jordanian 310 (83) 4413 (87) 4723 (86) Egyptian 14 (4) 140 (3) 154 (3) Palestinian 46 (12) 446 (9) 492 (9) Other 2 (1) 94 (2) 96 (2) Father’s nationality [no. (%)] 0.158 Jordanian 315 (84) 4485 (88) 4800 (88) Egyptian 17 (5) 155 (3) 172 (3) Palestinian 38 (10) 406 (8) 444 (8) Other 3 (1) 47 (1) 50 (1) Tobacco smoke exposure [no. (%)] Primary exposure 28 (8) 379 (7) 407 (7) 1.000 Secondary exposure 266 (71) 3616 (71) 3882 (71) 0.944 Any exposure 268 (72) 3665 (72) 3933 (72) 1.000 Location of prenatal care [no. (%)] MOH 83 (22) 818 (16) 901 (16) 0.002 UNRWA 76 (20) 1053 (21) 1129 (21) 0.943 Private sector 146 (39) 1687 (33) 1833 (34) 0.020 University 1 (< 1) 12 (< 1) 13 (< 1) 1.000 Other 3 (1) 20 (< 1) 23 (< 1) 0.441 None specified 111 (30) 2099 (41) 2210 (40) Time spent outdoors Median time (IQR) (hours/day) 0.5 (0.5–1.5) 1.0 (0.5–2.0) 1.0 (0.5–2.0) 0.568

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Table 1 Newborn characteristics by neonatal intensive care unit (NICU) admission in Amman, Jordan (concluded) Variable NICU Non-NICU Total P-value (n = 373) (n = 5093) (n = 5466) Use of supplements Took vitamin D during pregnancy [no. (%)] 72 (19) 1128 (22) 1200 (22) 0.224 Supplements taken [no. (%)] Folic acid 215 (58) 2351 (46) 2566 (47) < 0.001 Multivitamins 155 (42) 1140 (22) 1295 (24) < 0.001 Calcium 151 (40) 1436 (28) 1587 (29) < 0.001 Calcium with vitamin D 14 (4) 96 (2) 110 (2) 0.022 Vitamin D only 0 (0) 6 (< 1) 6 (< 1) 1.000 Iron 225 (60) 2309 (45) 2534 (46) < 0.001 Unknown vitamin 2 (1) 39 (1) 41 (1) 0.853 Other 6 (2) 29 (1) 35 (1) 0.036 Any vitamin D supplementation 162 (43) 1214 (24) 1376 (25) < 0.001 Received any vaccinations during pregnancy [no. (%)] 79 (21) 1216 (24) 1295 (24) 0.263 Mother’s medical history [no. (%)] Hyperparathyroidism 0 (0) 4 (< 1) 4 (< 1) 1.000 Diabetes 9 (2) 2 (< 1) 11 (< 1) < 0.001 Gestational diabetes 8 (2) 16 (< 1) 24 (< 1) < 0.001 Thyroid dysfunction 3 (1) 34 (1) 37 (1) 1.000 Renal failure 0 (0) 3 (< 1) 3 (< 1) 1.000 Heart disease 1 (< 1) 9 (< 1) 10 (< 1) 1.000 Asthma 0 (0) 38 (1) 38 (1) 0.177 Rheumatoid arthritis 15 (4) 105 (2) 120 (2) 0.021 Chronic disease requiring steroids 1 (< 1) 6 (< 1) 7 (< 1) 0.973 Hypertension 7 (2) 42 (1) 49 (1) 0.072 Gestational (pregnancy-induced) hypertension 21 (6) 71 (1) 92 (2) < 0.001 Total newborn vitamin D Vitamin D level (nmol/L) [median (IQR)] 3.5 (2.4–5.2) 3.5 (2.3–5.0) 3.5 (2.3–5.0) 0.269 Missing values [no. (%)] 39 (10) 1517 (30) 1556 (28)

IRQ = interquartile range; BMI = body mass index; MOH = Ministry of Health; UNRWA = United Nations Relief and Works Agency for Palestine Refugees in the Near East.

However, the median gestational age developed countries and are considered found to be lower than for those who of 36 weeks and birth weight of 2.2 kg non-viable. During the study period, the are extremely premature, this group were higher than median birth weight majority of newborns with a gestational has a greater need for NICU admis- of 2.0 kg and gestational age of 31–34 age < 26 weeks were categorized as non- sion, higher morbidity associated with weeks among neonates admitted to viable. This is consistent with the high organ immaturity and more long-term NICUs in North America and Europe 14.3% non-viable birth rate at Al-Bashir neurodevelopmental problems when (16–18). The majority of our neonates Hospital. Therefore, a further under- compared with term infants (19–27). would be considered late preterm in- standing of risk factors for premature A recent study at a military hospital in fants (34–36 weeks). A difference in birth Amman is needed to reduce the Amman, Jordan found that 72.7% of approach to care at the time of delivery rate of non-viable births, since these preterm births were late preterm in- may explain our older NICU cohort. neonates are less likely to be admitted fants and that these infants experienced For instance, infants that are extremely to the NICU. significantly higher morbidity and hos- premature do not receive the same ag- Although the morbidity and mor- pitalization than did term infants (28). gressive resuscitation that they would in tality of late-preterm infants has been Factors including male sex, maternal

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Table 2 Potential risk factors for neonatal intensive care unit admission, logistic regression model results in Amman, Jordan (n = 5466) Variable OR 95% CI P-value Newborn characteristics Sex Male 1.33 1.00–1.77 0.052 Gestational age (weeks) < 0.001 34 8.36 5.63–12.4 36 3.59 2.69–4.77 38 1.62 1.27–2.07 40 (Ref.) 1 42 0.78 0.50–1.23 Birth weight (kg) < 0.001 2 43.5 28.3–66.9 2.5 5.39 4.44–6.55 3 (Ref.) 1 3.5 1.39 1.21–1.60 Type of delivery < 0.001 Vaginal (Ref.) 1 Caesarean section 2.36 1.71–3.23 Month of birth < 0.001 May 2010 2.43 1.45–4.10 August 2010 (Ref.) 1 November 2010 0.46 0.32–0.66 February 2011 0.74 0.44–1.24 May 2011 2.15 1.40–3.30 Maternal characteristics Age (per 5 years) 1.02 0.92–1.14 0.669 Education 0.717 No education 0.80 0.36–1.75 Primary education 1.15 0.80–1.66 Secondary education (Ref.) 1 College/university 1.10 0.64–1.90 Location of prenatal care Any MOH clinic 1.53 0.94–2.49 0.090 Any UNRWA clinic 1.35 0.85–2.14 0.199 Any private sector clinic 1.17 0.74–1.83 0.501 Clothing practice 0.221 Head scarf only (Ref.) 1 European dress 3.37 0.73–15.6 Fully covered 1.21 0.78–1.87 Time spent outdoors (hours/day) 0.98 0.85–1.13 0.761 Tobacco smoke exposure Primary exposure 0.68 0.39–1.18 0.172 Secondary exposure 0.90 0.65–1.24 0.511 Use of supplements Any vitamin D supplementation 1.63 1.15–2.32 0.007

OR = odds ratio; CI = confidence interval; Ref = reference group. MOH = Ministry of Health; UNRWA = United Nations Relief and Works Agency for Palestine Refugees in the Near East.

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0 10 20 30 40 50 60 70 80 90 100 Points

Male Sex Female

Gestational age (weeks) 44 40 38 36 34 32 30 28 26 24 3.5 4 4.5 5 5.5 6 Birth weight (kg) 3 2.5 2 1.5 1 0.5 C−Section Delivery NSVD

Maternal age (years) 10 Secondary education Mother's education No education Ye s Any MOH prenatal care No Ye s Any UNRWA prenatal care No Ye s Any private sector prenatal care No Fully covered Mother's clothing practice Head scarf only

Hours mother spends outdoors per day 8 No Primary smoking exposure Ye s Ye s Secondary smoking exposure No Ye s Any vitamin D supplementation No Feb 11 May 11 Date of birth Nov 10 May 10

Total Points 0 20 40 60 80 100 120 140 160 180 200

Risk of NICU Admission 0.001 0.01 0.05 0.2 0.5 0.8 0.95 0.99 0.999

Figure 2 Nomogram of potential risk factors for neonatal intensive care unit (NIUC) admission in Amman, Jordan

age > 35 years and first birth were associ- preterm births in Amman is needed to NICU after adjusting for multiple ma- ated with preterm birth in a previous reduce the morbidity of this population. ternal and neonatal factors. These data study in Jordan (29). However, data Gestational age, birth weight and support studies in other countries, in on this topic are limited. Therefore, a delivery by caesarean section emerged where preterm delivery, multiple births further understanding of risk factors for as risk factors for admission to the and caesarean section were found to be

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Table 3 Neonatal intensive care unit (NICU) patient characteristics and outcomes by delivery type in Amman, Jordan Variable Vaginal Caesarean Total P-value (n = 162) (n = 156) (n = 318) Female sex 72 (44) 81 (52) 153 (48) 0.222 Gestational age 36 Gestational age (weeks) [median (IRQ)] 36 (35–37) 36 (34–37) 0.016 (34–37) Missing values [no. (%)] 2 (1) 2 (1) 4 (1) – Birth weight 2.3 Birth weight (kg) [median (IRQ)] 2.3 (2.–3) 2.3 (1.8–2.8) 0.039 (1.9–2.9) 1 Missing values [no. (%)] 0 (0) 1 (1) – < 1 Weight at 5 days (kg) [median (IRQ)] 2.11 (1.79–2.83) 1.90 (1.58–2.43) 2.00 (1.73–2.60) 0.045 Missing values [no. (%)] 110 (68) 101 (65) 211 (66) – Days in hospital [median (IRQ)] 3 (1–6) 4 (2–9) 3 (1–7) 0.002 Reason(s) for admission [no. (%)] Sepsis 15 (9) 16 (10) 31 (10) 0.912 Respiratory distress syndrome 105 (65) 107 (69) 212 (67) 0.552 Neonatal pneumonia 1 (1) 0 (0) 1 (< 1) 1.000 Prematurity 75 (46) 89 (57) 164 (52) 0.071 Heart disease 3 (2) 3 (2) 6 (2) 1.000 Congenital malformation 12 (7) 6 (4) 18 (6) 0.258 Overweight infant 8 (5) 9 (6) 17 (5) 0.936 Low birth weight infant 22 (14) 22 (14) 44 (14) 1.000 Jaundice 8 (5) 8 (5) 16 (5) 1.000 Low Apgar score 2 (1) 17 (11) 19 (6) < 0.001 Hypoglycaemia 3 (2) 1 (1) 4 (1) 0.642 Neonatal asphyxia 4 (2) 10 (6) 14 (4) 0.150 Other 55 (34) 44 (28) 99 (31) 0.325 Death 12 (7) 15 (10) 27 (8) – Apgar scores Apgar score at 1 min. [median (IRQ)] 7 (5–7) 6 (5–7) 7 (5–7) 0.339 Missing values [no. (%)] 131 (81) 10 (6) 141 (44) – Apgar score at 5 min. [median (IRQ)] 8 (7–8) 8 (6–8) 8 (7–8) 0.149 Missing values [no. (%)] 107 (66) 10 (6) 117 (37) – Supplement use by mother Vitamin D (nmol/L) [median (IRQ)] 3.5 (2.5–5.2) 3.5 (2.5–4.9) 3.5 (2.5–5.0) 0.945 C-reactive protein ever positive [no. (%)] 1.000 Missing 17 (10) 12 (8) 29 (9) – Negative 133 (92) 132 (92) 265 (92) – Positive 12 (8) 12 (8) 24 (8) – White blood cell counts 1st value (× 109 /L) [median (IRQ)] 13.9 (10.3–18.4) 13.1 (9.2–16.8) 13.2 (9.9–17.3) 0.047 Missing values [no. (%)] 8 (5) 0 (0) 8 (3) – NICU treatment Surfactant [no. (%)] 7 (4) 18 (12) 25 (8) 0.029 Antibiotics (days) [median (IRQ)] 3 (2–6) 4 (3–8) 4 (2–7) 0.002 Mechanical ventilation [no. (%)] 12 (7) 17 (11) 29 (9) 0.376 Mechanical ventilation (days) [median (IRQ)] 2 (2–3) 4 (1–9) 3 (1–6) – Nasal cannula [no. (%)] 48 (30) 69 (44) 117 (37) 0.010 Nasal cannula (days) [median IRQ)] 1 (1–2) 1 (1–3) 1 (1–2) – Oxyhood [no. (%)] 97 (60) 94 60 191 (60) 1.000 Oxyhood (days) [median (IRQ)] 1 (1–2) 1 (1–2) 1 (1–2) – Incubator [no. (%)] 56 (35) 52 (33) 108 (34) 0.909 Incubator (days) [median (IRQ)] 1 (1–2) 2 (1–2) 1 (1–2) – Mother’s complications [no. (%)] Gestational diabetes mellitus 7 (4) 15 (10) 22 (7) 0.101 Premature rupture of membranes 11 (7) 11 (7) 22 (7) 1.000 Pre-eclampsia 3 (2) 28 (18) 31 (10) < 0.001 IRQ = interquartile range.

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associated with NICU admission (30– as use of surfactant, oxygen by nasal can- on every neonate born during the study 34). The physiological immaturity as- nula and longer courses of antibiotics period. Some of the mothers we ap- sociated with young gestational age puts than neonates born by vaginal delivery. proached to join the prospective co- these infants at higher risk of respiratory This finding is consistent with Tita et al., hort chose not to participate, and there distress and in greater need for support. who found caesarean section prior to 39 were neonates unaccompanied by their Even among neonates delivered by cae- weeks to be associated with an increased mothers who we were unable to enrol. sarean section, gestational age remains a risk of adverse neonatal outcomes such We expect that our study estimate for stronger predictor of NICU admission as respiratory complications and ad- NICU admission of 6.8% is an underes- than rupture of membranes or trial of mission to the NICU (37). However, timate, given that the NICU admission labour before delivery (35). Maternal their study looked at elective caesarean rate for the hospital was much higher at factors found to predict NICU admis- section, while all of the caesarean sec- 19.8%. This implies that mothers with sion in other studies include age, race tions in our study were non-elective. infants in the NICU were less likely to (16), body mass index (36), premature It is currently unclear whether this is enrol in our study. If refusals among rupture of membranes, antepartum the result of an obstetric practice that this population were random, then our haemorrhage and medical disorders is quicker to proceed to caesarean sec- assessment of risk factors would be during pregnancy (32,33). Brown et tion with any sign of distress or because unbiased. If mothers with sicker babies al. suggested that placental ischaemia our cohort is composed of higher risk refused, then our results may be biased and endocrine abnormalities associated pregnancies. Another Jordanian study towards the null as our study NICU with these conditions work as biologi- concluded that an over-diagnosis of population would be more like the gen- cal determinants of preterm birth that fetal distress and dystocia was one cause eral population. If mothers with sicker act through and with gestational age to of the unnecessarily high caesarean sec- babies were more likely to participate, produce poor outcomes (34). In our tion rate at King Hussein Medical Cen- then our results would be biased away cohort, maternal age and ethnicity were tre in Amman (38). These data suggest from the null as our study NICU popu- not risk factors for NICU admission. that working to decrease the number of lation would be much different from Interestingly, birth in the month of caesarean sections may be an effective the general population. We believe that May was also associated with higher way to decrease admission to the NICU if a bias exists, it would exist towards odds of admission to the NICU. No and the associated morbidities. Investi- the null. However, it is possible that the increase in the rate of caesarean sections gators in China implemented a 6-year highest risk neonates were not included was noted during this time period, mak- programme aiming to decrease the in our study. Of note, the NICU was ing this unlikely to be the explanation. It number of caesarean sections, through undergoing renovations between May is not known why birth in May is a risk educational sessions for the entire ob- 2010 and July 2011, which decreased factor and therefore this issue merits ad- stetric care staff, removal of financial the overall birth census during this time ditional investigation to identify a cause incentives for performing caesarean period. that can be targeted to decrease NICU sections, daily review of the indications Other limitations of our study were admission. for each case and improvements in that we were unable to obtain the medi- In our cohort of NICU admissions, monitoring technology. These inter- cal record of every neonate that was there was a significantly higher caesar- ventions resulted in a decrease in the admitted to the NICU during our study ean section rate among the neonates primary caesarean section rate by an an- period. The surveys used in prospec- admitted to the NICU compared with nual average of 20%, with a significantly tive data collection relied on maternal non-NICU neonates. Our caesarean lower rate in the post-intervention time self-reporting, making them subject to section rate of 49% for neonates admit- period than the pre-intervention period recall and response bias. Finally, the ted to the NICU is similar to a study (39). Therefore, further investigation of hospital’s use of paper charts rather than in the United States that found a 50% the indications for caesarean section in electronic medical records resulted in caesarean section rate in their NICU Jordan is needed. If it is found that inap- missing data in some of the charts that cohort (24). In our study, median propriate indications are used, an effort were retrospectively reviewed. How- gestational age and birth weight were similar to the Chinese investigators’ ever, the major strength of the study is lower in neonates delivered by caesar- could be implemented to help reduce the inclusion of a large neonatal cohort ean section compared to those born by unnecessary caesarean sections and the with both maternal and newborn data. vaginal delivery. This weight difference associated neonatal complications. This study represents the first -ef persisted 5 days after birth. In addition, There were limitations of our study. fort in the Middle East to describe a neonates born by caesarean section re- The most important was that we were large cohort of neonates admitted to quired more intensive treatment, such unable to obtain complete information the NICU and to estimate risk factors

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for admission. Our results indicate births among the NICU neonates, and may be an important step in reducing that the majority of neonates in the these neonates required more intensive neonatal morbidity and mortality in Al-Bashir Hospital NICU are late care while in the NICU. Thus, further Jordan. These data serve as a starting preterm infants. Gestational age, birth investigation into risks for preterm birth point and the study highlights the need weight, caesarean section and birth in and why births in May was associated for a targeted prospective study in the the month of May were the most in- with NICU admission are needed. Ad- Arab world to understand risk factors fluential risk factors for admission to ditionally, addressing obstetric prac- for admission to the NICU. the NICU. Additionally, there was a tices to reduce the number of preterm Funding: None much higher rate of caesarean section infants delivered by caesarean section Competing interests: None declared.

References

1. Bettegowda V, Lackritz E, Petrini J. Epidemiologic trends in 13. Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Con- perinatal data. Chapter 3. In: Toward improving the outcome de JG. Research electronic data capture (REDCap) – a of pregnancy III. White Plains (NY): March of Dimes Founda- metadata-driven methodology and workflow process for tion; 2010 (http://www.marchofdimes.org/materials/to- providing translational research informatics support. J Bi- ward-improving-the-outcome-of-pregnancy-iii.pdf, accessed omed Inform. 2009 Apr;42(2):377–81. PMID:18929686 10 January 2016). 14. Harrell F. Regression modeling strategies: with applications to 2. Tatad AM, Frayer WW. Trends in the NICU: a review of 25 linear models, logistic regression, and survival analysis. New years’ experience. Am J Perinatol. 2003 Nov;20(8):441–6. York: Springer; 2001. PMID:14703592 15. R: a language and environment for statistical computing. Vi- 3. 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The impact of preterm birth on hospital inpatient PMID:22579125 admissions and costs during the first 5 years of life. Pediatrics. 9. Jordan: WHO statistical profile [Internet]. Geneva: World 2003 Dec;112(6 Pt 1):1290–7. PMID:14654599 Health Organization; 2013 (http://www.who.int/gho/coun- 23. Melamed N, Klinger G, Tenenbaum-Gavish K, Herscovici T, tries/jor.pdf, accessed 10 January 2016). Linder N, Hod M, et al. Short term neonatal outcome in low- 10. Country cooperation strategy for WHO and Jordan 2008– risk spontaneous, singleton, late preterm deliveries. Obstet 2013. Cairo: World Health Organization Regional Office for Gynecol. 2009 Aug;114(2 Pt 1):253–60. PMID:19622985 the Eastern Mediterranean; 2009 (http://applications.emro. 24. Mally PV, Hendricks-Muñoz KD, Bailey S. Incidence and who.int/docs/CCS_Jordan_2010_EN_14473.pdf, accessed 10 etiology of late preterm admissions to the neonatal intensive January 2016). care unit and its associated respiratory morbidities when com- 11. Khoury SA, Mas’ad DF. Causes of infant mortality in Jordan. pared to term infants. Am J Perinatol. 2013 May;30(5):425–31. Saudi Med J. 2002 Apr;23(4):432–5. PMID:11953770 PMID:23096053 12. Khuri-Bulos N, Lang RD, Blevins M, Kudyba K, Lawrence L, 25. Tsai ML, Lien R, Chiang MC, Hsu JF, Fu RH, Chu SM, et al. Preva- Davidson M, et al. Vitamin D deficiency among newborns lence and morbidity of late preterm infants: current status in in Amman, Jordan. Glob J Health Sci. 2014 Jan;6(1):162–71. a medical center of Northern Taiwan. Pediatr Neonatol. 2012 PMID:24373276 Jun;53(3):171–7. PMID:22770105

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26. McLaurin KK, Hall CB, Jackson EA, Owens OV, Mahadevia PJ. tify late preterm infants at risk for neonatal intensive care unit Persistence of morbidity and cost differences between late- admission. J Obstet Gynaecol Res. 2015 May;41(5):680–8. preterm and term infants during the first year of life. Pediatrics. PMID:25420697 2009 Feb;123(2):653–9. PMID:19171634 34. Brown HK, Speechley KN, Macnab J, Natale R, Campbell MK. 27. Petrini JR, Dias T, McCormick MC, Massolo ML, Green NS, Es- Neonatal morbidity associated with late preterm and early cobar GJ. Increased risk of adverse neurological development term birth: the roles of gestational age and biological determi- for late preterm infants. J Pediatr. 2009 Feb;154(2):169–76. nants of preterm birth. Int J Epidemiol. 2014 Jun;43(3):802–14. PMID:19081113 PMID:24374829 28. Abu-Salah O. Unfavourable outcomes associated with late 35. Yee W, Amin H, Wood S. Elective cesarean delivery, neonatal preterm birth: observations from Jordan. J Pak Med Assoc. 2011 intensive care unit admission, and neonatal respiratory dis- Aug;61(8):769–72. PMID:22355999 tress. Obstet Gynecol. 2008 Apr;111(4):823–8. PMID:18378740 29. Mohammad K, Abu Dalou A, Kassab M, Gamble J, Creedy DK. 36. Crane JM, Murphy P, Burrage L, Hutchens D. Maternal and Prevalence and factors associated with the occurrence of pre- perinatal outcomes of extreme obesity in pregnancy. J Obst term birth in Irbid governorate of Jordan: a retrospective study. Gynaecol Can. 2013 Jul;35(7):606–11. PMID:23876637 Int J Nurs Pract. 2015 Oct;21(5):505–10 PMID:25213160 37. Tita AT, Landon MB, Spong CY, Lai Y, Leveno KJ, Varner MW, 30. Barfield W. Neonatal intensive-care unit admission of infants et al.; Eunice Kennedy Shriver NICHD Maternal-Fetal Medicine with very low birth weight—19 States, 2006. MMWR Morb Units Network. Timing of elective repeat cesarean delivery Mortal Wkly Rep. 2010 Nov 12;59(44):1444–7. PMID:21063275 at term and neonatal outcomes. N Engl J Med. 2009 Jan 31. Gyamfi-Bannerman C, Fuchs KM, Young OM, Hoffman 8;360(2):111–20. PMID:19129525 MK. Nonspontaneous late preterm birth: etiology and out- 38. Dabbas M, Al-Sumadi A. Cesarean section rate: much room comes. Am J Obstet Gynecol. 2011 Nov;205(5):456.e1–6. for reduction. Clin Exp Obstet Gynecol. 2007;34(3):146–8. PMID:22035950 PMID:17937087 32. Dimitriou G, Fouzas S, Georgakis V, Vervenioti A, Papado- 39. Runmei M, Terence T L, Yonghu S, Hong X, Yuqin T, Bailuan L, poulos VG, Decavalas G, et al. Determinants of morbidity in et al. Practice audits to reduce caesareans in a tertiary referral late preterm infants. Early Hum Dev. 2010 Sep;86(9):587–91. hospital in south-western China. Bull World Health Organ. PMID:20729014 2012 Jul 1;90(7):488–94. PMID:22807594z 33. Phaloprakarn C, Manusirivithaya S, Boonyarittipong P. Risk score comprising maternal and obstetric factors to iden-

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Trend of bacterial meningitis in Bahrain from 1990 to 2013 and effect of introduction of new vaccines N. Saeed,1 H. AlAnsari,2 S. AlKhawaja,2,3 J.S. Jawad,4 K. Nasser 3 and E. AlYousef 5

اجتاه التهاب السحايا اجلرثومي يف البحرين من عام 1990إىل عام ،2013 وتأثري إدخال لقاحات جديدة نرمني سعيد، هدى األنصاري، صفاء اخلواجة، جليلة جواد، كربى نارص، إبتهال اليوسف اخلالصــة: يعتــرب التهــاب الســحايا مــن بــني األمــراض ُاملعديــة املميتــة الـــ 10 األكثــر ً شــيوعاعــى مســتوى العــامل. وهيــدف هــذا التحليــل االســتعادي حلــاالت التهــاب الســحايا املبلــغ عنهــا يف البحريــن إىل تقييــم االجتــاه يف وقــوع التهــاب الســحايا اجلرثومــي مــن عــام 1990إىل عــام 2013، قبــل وبعــد إدخــال لقاحــات جديــدة. لقــد كانــت املســببات فريوســية يف %73.1 مــن حــاالت التهــاب الســحايا الـــ 1455 التــي أبلــغ عنهــا خــال فــرة الدراســة، وجرثوميــة يف % 26.9مــن احلــاالت )التهــاب ســحايا ســي %8.3، وبالعقديــة الرئويــة %4.9، وباملســتدمية النزليــة 3.6%، وبالنيرسيــة الســحائية % (.1.7 وكانــت هنــاك ذروة لظهــور حــاالت التهــاب الســحايا يف العامــني 1995-1996. وأظهــر وقــوع التهــاب الســحايا بســبب املســتدمية النزليــة والنيرسيــة الســحائية ًانخفاضــا ً ملحوظــابعــد إدخــال اللقاحــات املوافقــة لــكل منهــا يف عامــي 1998 و2001 عــى التــوايل، وأصبحــت العقديــة الرئويــة الكائــن احلــي الســائد بعــد املتفطــرة الســلية. إن االجتــاه املتغــري يف مســببات التهــاب الســحايا اجلرثومــي يشــري إىل رضورة إجــراء دراســة إلدخــال تعديــات عــى برنامــج التطعيــم؛ مثــل: لقــاح املكــورات الرئويــة للبالغــني، ال ّســيم الفئــات عاليــة اخلطــورة.

ABSTRACT Meningitis is among the 10 commonest infectious causes of death worldwide. This retrospective analysis of reported cases of meningitis in Bahrain aimed to assess the trend in the incidence of bacterial meningitis from 1990 to 2013, before and after the introduction of new vaccines. Of 1455 reported cases of meningitis during the study period 73.1% were viral and 26.9% were bacterial etiology (tuberculous meningitis 8.3%; Streptococcus pneumoniae 4.9%, Haemophilus influenzae 3.6% and Neisseria meningitidis 1.7%). There was a peak of meningitis cases in 1995–1996. The incidence of meningitis due to H. influenzae and N. meningitidis showed a marked reduction after the introduction of the corresponding vaccines in 1998 and 2001 respectively, and S. pneumoniae became the predominant organism after Mycobacterium tuberculosis. The changing trend in the etiology of bacterial meningitis points to the need to study vaccination programme modifications, such as pneumococcal vaccine for the adult population, especially high-risk groups.

Tendances de la méningite bactérienne à Bahreïn entre 1990 et 2013 et effets de l’introduction de nouveaux vaccins

RÉSUMÉ La méningite fait partie des 10 causes de décès par infection les plus courantes dans le monde. La présente analyse rétrospective des cas de méningite notifiés à Bahreïn visait à mesurer la tendance de l’incidence de la méningite bactérienne entre 1990 et 2013, avant et après l’introduction de nouveaux vaccins. Sur 1 455 cas de méningite rapportés au cours de la période d’étude, 73,1 % étaient d’étiologie virale et 26,9 % d’étiologie bactérienne (méningite tuberculeuse 8,3 % ; Streptococcus pneumoniae 4,9 %, Haemophilus influenzae 3,6 % et Neisseria meningitidis 1,7 %). Un pic de cas de méningite est survenu entre 1995 et 1996. L’incidence des méningites dues à H. influenzae et N. meningitidis a marqué une nette réduction après l’introduction des vaccins correspondants en 1998 et 2001 respectivement, et S. pneumoniae est devenu l’organisme prédominant après Mycobacterium tuberculosis. Ce changement de tendance dans l’étiologie de la méningite bactérienne souligne le besoin d’étudier les possibilités de modifications du programme de vaccination, telle que la vaccination antipneumococcique de la population adulte, notamment pour les groupes à haut risque.

1Department of Pathology; 2Department of Infection Control; 3Communicable Disease Section; 4Immunization Section, Ministry of Health, Bahrain. 5Department of Internal Medicine, Salmaniya Medical Centre, Bahrain (Correspondence to N. Saeed: [email protected]). Received: 25/08/15; accepted: 10/01/16

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Introduction evaluation of the impact of new vac- consciousness, signs of meningeal ir- cines by considering the geographical ritation or petechial/purpuric rash) Despite improvements in its treat- variations in incidence of the causative or bulging fontanel in infants. Cases ment, bacterial meningitis continues pathogens across countries. It could are then stratified into either probable to have high mortality and morbidity also help to detect a need for modifi- (when combined with turbid CSF) or rates worldwide. Meningitis is among cation of the vaccination protocol if confirmed (when accompanied by pos- the 10 most common infectious the efficacy of the current protocol is itive CSF culture) according to WHO causes of death and is responsible for inadequate (5). According to the best case definitions and laboratory criteria approximately 135 000 deaths annu- of our knowledge, there have been no (6). Active surveillance for meningitis ally throughout the world. Significant previous surveillance studies to monitor cases was done through regular tracing neurological sequelae are frequently the efficacy of the current vaccination and review of medical records based on encountered among the survivors (1). protocols applied in Bahrain to prevent International Classification of Diseases Streptococcus pneumoniae and Neisseria bacterial meningitis. This stimulated us coding for inpatients admitted to Sal- meningitidis are the main pathogens of to conduct this study to assess the trend maniya Medical Complex, which is the community-acquired bacterial menin- and the temporal relationship between only government tertiary care hospital gitis in adults. However, the epidemiol- the introduction of new vaccines and concerned with treatment of such cases ogy of bacterial meningitis continues the change in the incidence of bacterial in the country. In the current study, to shift with the ongoing introduction meningitis over 24 year-period 1990 to we included only the confirmed cases. of vaccines against the most common 2013. Meningitis cases were also classified by pathogens of bacterial meningitis (2). etiology into viral or bacterial and type Bahrain is an island on the east coast of bacterium. of the Arabian Peninsula with a popula- Methods tion of 1.31 million in the year 2013. Im- Data analysis Study design and data source migrants make up about 55% of the total Data pertaining to all cases were entered population (3). Bahrain has one of the This study was a retrospective analysis into a MicrosoftExcel database. The data most efficient health care systems in the of reported cases of bacterial meningitis were analysed separately for the trend of World Health Organization (WHO) in Bahrain from 1990 to 2013. Data change in the incidence over the last 24 Eastern Mediterranean Region. Bahrain were retrieved from the national surveil- years using TexaSoft WINKS SDA soft- implements a comprehensive expanded lance system of communicable diseases, ware 2007 (6th edition). Comparisons immunization programme with excel- which is managed by the Department of between the number of meningitis cases lent coverage rates (> 95%) for most Public Health at the Ministry of Health in the periods before and after the in- routine childhood vaccines, including of Bahrain. The meningitis surveillance troduction of specific vaccines into the those against S. pneumoniae, N. menin- includes both passive and active surveil- Bahrain vaccination programme were gitidis and Haemophilus influenzae. H. lance systems. The research and eth- performed with Student t-test, with P < influenzae vaccine was introduced in ics committee of Salmaniya Medical 0.05 considered statistically significant. routine childhood vaccines in 1998, and Complex approved the study. This was bivalent meningococcal AC vaccine a purely record-based study with no was introduced in 1995 for children ethical issues and no consent was taken. Results aged 2 years and for those travelling for pilgrimage. However, it was replaced in Data collection All types of meningitis 2000 by the quadrivalent meningococ- Passive surveillance includes man- Table 1 shows the total number of cases cal ACYW vaccine. One year later, in datory reporting for all the clinically of meningitis reported in Bahrain from 2001, the conjugated pneumococcal suspected and confirmed meningitis 1990 to 2013 and the number of cases vaccine was introduced for high-risk cases reported from all government and by etiology. The total number of men- people and was incorporated into the private hospitals in the country. All the ingitis cases during the study period routine childhood vaccination schedule microbiology laboratories in Bahrain was 1437. Viral meningitis accounted by 2008 (4). also report any positive cerebrospinal for 1051 (73.1%) cases and bacte- Epidemiological surveys are impor- fluid (CSF) culture from laboratory rial meningitis for 386 (26.9%) cases. tant to document the incidence of bac- confirmed cases. Clinically suspected Tuberculous meningitis was the most terial meningitis in the periods before cases are defined as illness with sudden frequent bacterial cause, detected in 122 and after the introduction of vaccines onset of fever (> 38.5 °C) and one of patients (8.5%), followed by S. pneumo- to a country. This could allow proper the following (neck stiffness, altered niae (70 cases; 4.9%), H. influenzae (52

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Table 1 Number of cases of meningitis in Bahrain over the years 1990–2013, by etiology Year Total Viral Bacterial Subtype of bacterial meningitis Pneumococcal Meningococcal H. influenzae Staphylococcal Tuberculous Other type b 1990 22 7 15 4 4 2 0 5 0 1991 45 32 13 4 0 4 1 1 3 1992 43 14 29 6 4 5 1 4 9 1993 26 10 16 2 1 3 0 4 6 1994 31 20 11 2 2 2 0 4 1 1995 310 285 25 2 0 9 0 10 4 1996 232 199 33 1 1 11 0 8 12 1997 44 25 19 1 2 7 0 2 7 1998 46 27 19 5 4 4 0 5 1 1999 55 40 15 3 1 2 0 6 3 2000 68 54 14 2 1 3 1 6 1 2001 45 35 10 2 3 0 0 1 4 2002 40 32 8 4 0 0 0 2 2 2003 46 38 8 5 0 0 0 3 0 2004 40 26 14 3 0 0 1 10 0 2005 22 12 10 2 0 0 3 2 3 2006 57 39 18 4 0 0 0 7 7 2007 38 27 11 2 0 0 1 6 2 2008 33 15 18 4 0 0 0 6 8 2009 47 27 20 1 0 0 0 13 6 2010 37 23 14 3 1 0 2 5 3 2011 10 0 10 3 0 0 0 3 4 2012 37 18 19 4 0 0 1 7 7 2013 63 46 17 1 0 0 1 2 13 Total 1437 1051 386 70 24 52 12 122 106

cases; 3.6%) and then N. meningitidis Bacterial meningitis gradually to 0.1 per 100 000 in 2013. (24 cases; 1.7%). Figure 2 shows the incidence of Figure 3 shows the trends in incidence Figure 1 illustrates the trend of the pneumococcal, meningococcal and in children only. The red arrows refer viral and bacterial meningitis during Haemophilus influenzae meningitis in to the timing of various stages of intro- the study period. The average incidence both adults and children over the 24- duction of pneumococcal conjugate of meningitis between 1990 and 2000 year period. Figure 3 shows the trend in vaccine. The first arrow (2001) refers ranged from around 5 to 10 cases per the incidence of tuberculous and total to the introduction of the vaccine to 100 000 population (Figure 1). The bacterial meningitis and of pneumococ- high-risk children, while the second red trend was almost stable for viral and cal, meningococcal and Haemophilus arrow (2008) indicates the expansion bacterial meningitis during the study influenzae meningitis in children only. of the 7 valent pneumococcal conjugate period. However, the incidence showed The charts illustrate the decline in the vaccine to include all infants through a marked peak in 1995 and 1996, reach- incidence of different types of bacterial routine childhood vaccination (at ages ing 50 cases per 100 000 population, meningitis after the introduction of the 2, 4, 6 and 18 months). The third red mostly due to viral and H. influenzae corresponding vaccines. arrow (2010) refers to replacing the 7 meningitis. From 2001, there was Pneumococcal meningitis polyvalent vaccines with 13 polyvalent gradual decline in the incidence of men- Figure 2 shows that the incidence of vaccines for children. The fourth red ingitis from 6.7 cases per 100 000 in pneumococcal meningitis was 1 per arrow (2013) refers to the introduction 2001 to 5.0 cases per 100 000 in 2013 100 000 population at the beginning of 13 polyvalent vaccines for adults aged (Figure 1). of study period in 1990 and dropped ≥ 50 years.

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350

300

250 Pneumococcal Meningococcal

200 H. influenzae Staphlococcal Tuberculous 150 Other Bacterial

100 Viral Total

50

0

Figure 1 Annual incidence of total, viral and bacterial meningitis per 100 000 population in Bahrain over the years 1990–2013

Figure 4 shows the percentage of before 2008 were in children. However, reached a peak of 1.9 cases per 100 000 paediatric versus adult cases of pneumo- the proportion of paediatric cases with in 1996 with a cluster of cases and a coccal meningitis. There was significant pneumococcal meningitis gradually possible outbreak. reduction of the number of reported decreased to 62% after introduction of With introduction of the H. influen- cases of pneumococcal meningitis from the pneumococcal vaccine. zae conjugate vaccine to routine child- 58 cases before the introduction of Haemophilus meningitis hood vaccination in 1998 (shown by pneumococcal vaccine in 2008 to only the green arrow on the chart) there was A total of 52 cases of H. influenzae 12 cases from 2009 to 2013 after intro- a marked reduction of the incidence of meningitis were reported during the duction of the vaccine (Table 1). Four reported cases to reach zero after 2001 24-year period of the study (Table 1). cases occurred in children (< 14 years where there was no single reported case Most cases of H. influenzae meningitis old); all of them were infants below of H. influenzae meningitis in Bahrain. the age of 1 year, and 2 of them were (44 cases) were reported before the unvaccinated 5-day-old neonates with introduction of H. influenzae vaccine for Meningococcal meningitis positive blood and CSF culture. Three childhood in 1998. In 1995, there were There were 24 cases of meningococcal cases were 7, 8 and 11 months old; 2 of 9 cases with H. influenzae meningitis meningitis reported during the study them had received the recommended and 3 cases with other unknown bacte- period (Table 1). Figure 2 shows that pneumococcal vaccine on time (at 2, 4 rial causes, while in 1996 11 cases with the incidence of meningococcal menin- and 6 months of age). The third case was H. influenzae meningitis were reported gitis was 0.83 per 100 000 population in an immigrant non-Bahraini infant who among children aged 0–4 years (15 1990 and that this fluctuated annually had not previously received pneumo- per 100 000) and 9 cases with other until 2001. coccal vaccination as this vaccine was unknown bacterial causes with negative Figure 3 showed the trend of menin- not included in the routine vaccination culture and no identification. gococcal meningitis in children and the schedule in her original country. It is Figure 2 shows that the incidence related decline in its incidence related to also worth mentioning that all the cases of H. influenzae meningitis was 0.4 cases the introduction of the corresponding of pneumococcal meningitis recorded per 100 000 population in 1990, which vaccine. The first blue arrow (1995)

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12

Pneumococcal

10 Meningococcal H. influenzae

8

6

4

2

0

1991 2011 1990 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2012 2013

Year

Figure 2 Annual incidence of pneumococcal, meningococcal and Haemophilus influenzae bacterial meningitis per 100 000 population in Bahrain over the years 1990–2013. Arrows indicate dates of introduction of specific vaccines into the national programme of immunization (red arrows = various stages of introduction of pneumococcal conjugate vaccine; green arrow = introduction of H. influenzaconjugate vaccine; blue arrows = various stages of introduction of meningococcal vaccine)

refers to the timing of introduction of ACWY), except in 2010 when there the overall annual incidence of meningi- meningococcal AC vaccine routinely 1 case of meningococcal meningitis tis (bacterial and viral) during the study for children at age 2 years and for hajj reported in a 44-year-old Bahraini male. period from 1990 to 2013. The overall pilgrims, while the second blue arrow Although the patient had no known risk annual incidence ranged from 5 to 10 per (2000) refers to the replacement of factor or travel history, he was working 100 000 population, which is close to the meningococcal AC by meningococcal at the airport and we cannot exclude the incidence in nearby Gulf Cooperation ACWY polysaccharide for the same possibility of exposure to an infected Council (GCC) countries such as Qatar target group, and the third blue arrow traveller. (10 per 100 000) (7) and Oman (3 to (2013) indicates the change from 8.4 per 100 000) (8), but much higher quadrivalent meningococcal polysac- than observed in United Arab Emirates charide to the meningococcal ACWY Discussion (1 to 2.2 per 100 000) (9). conjugate for children aged 2 years, hajj We noted a peak number of re- pilgrims and high-risk groups. There The study aimed to investigate the an- ported confirmed cases with meningitis were no reported cases of meningo- nual trends and the effect of vaccination during 1995 and 1996, mostly due to coccal meningitis after 2002 (1 year on the incidence of bacterial meningitis viral and H. influenzae meningitis. This after the introduction of meningococcal in Bahrain. It showed a gradual decline in outbreak was the stimulus to introduce

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45 Total bacterial Tuberculous 40 Pneumococcal

35 H. influenzae

30 Meningococcal

25

20

15

10

5

0

Figure 3 Annual incidence of pneumococcal, meningococcal, Haemophilus influenzae, tuberculous and total bacterial meningitis per 100 000 children in Bahrain over the years 1990–2013. Arrows indicate dates of introduction of specific vaccines into the national programme of immunization (red arrows = various stages of introduction of pneumococcal conjugate vaccine; green arrow = introduction of H. influenzaeconjugate vaccine; blue arrows = various stages of introduction of meningococcal vaccine)

the H. influenzae type b (Hib) vaccine in to H. influenzae early after the introduc- H. influenzae, N. meningitidis and S. pneu- 1998 as a part of the 5-antigen vaccine tion of vaccine has been also observed in moniae (16). (against diphtheria, tetanus, pertussis, other nearby countries from the GCC N. meningitidis is responsible for seri- hepatitis B and H. influenzae type b) region as well other developed counties ous cases of meningitis and fulminant (10). (11). For example, in Kuwait, H. influ- septicaemia and is also a concern due The epidemiology of bacterial men- enzae was responsible for nearly half of to the characteristic dynamic nature ingitis in Bahrain continues to change the meningitis cases at the early 1990s, of the disease, both in its tendency to with the implementation of vaccination prior to the introduction of routine Hib occur in outbreaks and epidemics as strategies that target the most common vaccination. However, it was replaced well as the fact that the most prominent community-acquired pathogens. Dur- by S. pneumoniae as the leading causative disease-causing serogroups can change ing the study period (1990–2013), the agent for bacterial meningitis in Kuwait in a given region over a period of only most pivotal changes were observed after implementation of the successful few years (17). The current study also with the introduction of H. influenzae Hib vaccination policy (12). The same revealed a great reduction in the in- vaccines in 1998 and N. meningitidis vac- observation was also noted worldwide. cidence of meningococcal meningitis cine in 2000. Introduction of these two In the United States of America there in Bahrain from 0.83 per 100 000 in vaccines has been associated with a strik- was a significant decline in the incidence 1990 followed by a fluctuating pattern ing reduction in the incidence of both of H. influenzae meningitis over all States until 2001, which then reached zero H. influenzae and N. meningitidis, and from 0.10 per 100 000 population in incidence after 2002, 1 year after the since the year 2000 there was no single 1997 to 0.058 per 100 000 in 2010 (13– introduction of meningococcal ACWY reported case of H. influenzae and since 15). England showed also significant polysaccharide for children. However, 1 2002 onward there was only 1 reported reduction in hospital admission rates case of meningococcal meningitis was case of N. meningitidis meningitis. This for childhood invasive bacterial disease reported in a 44-year-old healthy male temporal relationship and the marked including meningitis after the intro- adult in 2010 with no history of travel or reduction in the rate of meningitis due duction of conjugate vaccines against contact with sick patients with a similar

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100

90

80

70

60

% 50 <14 years (%) >14 years (%) 40

30

20

10

0

1991 2011 1990 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2012 2013

Figure 4 Percentage of paediatric versus adult cases of pneumococcal meningitis in Bahrain over the years 1990–2013

illness. Such a major reduction in the region such as the USA also reported the among the paediatric age group, and incidence of meningococcal meningitis efficacy of the meningococcal vaccine, adults became the main target. This after the introduction of meningococcal with a great impact of the vaccine on shift may indicate a need to improve the ACWY vaccine and without changes reduction of the incidence of meningo- vaccination strategy, especially for high- in the meningitis control programme coccal disease (19). risk adults in Bahrain, given that many in our country is an indicator of the ad- Our study also illustrated a signifi- Bahrainis have sickle-cell disease which equacy and efficiency of the country’s cant drop in the incidence of S. pneumo- poses a significant risk of invasive pneu- vaccination policy. Similar data in other niae meningitis in Bahrain from 1 per mococcal disease. Our finding agrees GCC countries showed a reduction of 100 000 population at the beginning of with the work of Castelblanc et al., who meningococcal disease but to a lesser de- study period in 1990 to 0.1 per 100 000 observed a similar reduction in the inci- gree than observed in the current study in 2013. Yet it became the leading cause dence of S. pneumoniae meningitis and in Bahrain. Bahrain has a small popula- of bacterial meningitis (not considering a change in its epidemiological pattern tion which allows adequate implementa- tuberculous meningitis) in Bahrain, re- with a reduction of incidence from 0.81 tion of the vaccination programme, with placing H. influenzae and N. meningitidis per 100 000 in 1997 to 0.3 per 100 000 a direct impact of the vaccine on the after the striking reduction of these in 2010. However, they showed a con- target population as well as an indirect two organisms as a cause of bacterial sistent reduction in incidence in all protection of others due to a decrease in meningitis following the introduction age groups, with a greater reduction in the risk of disease contact, reduced trans- of the corresponding vaccines. The age children younger than 18 years of age mission rate and increase herd immunity distribution of S. pneumoniae meningitis (20). The same finding was also noted in the community. We noted that Oman showed significant differences between in a similar study in South Africa, which and Qatar all reported incidence rates 1990 and 2013. The disease was more showed a substantial decrease in the below 2 per 100 000, with the exception frequent in the paediatric age group incidence of invasive pneumococcal of a few higher rates in the mid-1980s (< 14 years of age) at the beginning of disease, particularly among children, (18). However, we cannot compare our the study; but after integrating the S after the introduction of pneumococ- results with those from Qatar as their pneumoniae vaccine into the extended cal vaccine into the routine childhood study included only children aged < 12 immunization programme for children schedule (21). The expansion of the years. Other countries outside the Gulf the disease started to be less common vaccine to adults and elderly people was

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recommended and supported by other the emergence of non-vaccine sero- cases, provide evidence of the efficacy of worldwide studies for further reduction types and would have informed possible the childhood vaccination programme of the rate of invasive pneumococcal modifications to our vaccine policy. in Bahrain against both H. influenzae disease (22–25). and N. meningitidis. At the same time, The limitation of our study was that it stimulates us to study the possibil- we did not know the serotypes of pneu- Conclusion ity of modification to the vaccination mococcal isolates causing pneumococ- programme, such as including pneu- cal meningitis after incorporation of The significant reduction of invasiveH. mococcal vaccine for the adult popula- pneumococcal vaccine into the routine influenzae meningitis since 2000, and tion, especially for high-risk groups, to childhood schedule. This would have the parallel resurgence of S. pneumoniae prevent invasive pneumococcal disease. enabled us to capture a decrease or near as the main cause of bacterial meningitis Funding: None. disappearance of vaccine serotypes or with an increased proportion of adult Competing interests: None declared.

References

1. Scheld WM, Koedel U, Nathan B, Pfister HW. Pathophysiology 14. Dery MA, Hasbun R. Changing epidemiology of bacterial men- of bacterial meningitis: mechanism(s) of neuronal injury. J Infect ingitis. Curr Infect Dis Rep. 2007 Jul;9(4):301–7. PMID:17618550 Dis. 2002 Dec 1;186 Suppl 2:S225–33. PMID:12424702 15. Thigpen MC, Whitney CG, Messonnier NE, Zell ER, Lynfield R, 2. Shah SF, Nadeem S, Farooq A, Bener A. Emerging trend in the Hadler JL, et al.; Emerging Infections Programs Network. Bacte- epidemiology of meningitis in Qatar. J Coll Physicians Surg Pak. rial meningitis in the United States, 1998–2007. N Engl J Med. 2008 Apr;18(4):259-60. PMID:18474169 2011 May 26;364(21):2016–25. PMID:21612470 3. Population and demographics [Internet]. Manama, Bahrain: 16. Martin NG, Sadarangani M, Pollard AJ, Goldacre MJ. Hospital Ministry of Information Affairs (www.mia.gov.bh/en/Kingdom- admission rates for meningitis and septicaemia caused by of-Bahrain/Pages/Population-and-Demographic-Growth. Haemophilus influenzae, Neisseria meningitidis, and Strep- aspx, accessed 19 January 2016). tococcus pneumoniae in children in England over five dec- 4. Six countries have decided to routinely immunise children ades: a population-based observational study. Lancet Infect against pneumococcal disease with Prevenar. PharmacoEco- Dis. 2014 May;14(5):397–405. 10.1016/S1473-3099(14)70027-1 nomics & Outcomes News. 2008 Jul;558(1):4. PMID:24631222 5. Travasso C. Better surveillance and vaccine coverage are need- 17. Hausdorff WP, Hajjeh R, Al-Mazrou A, et al. The epidemiology ed to eliminate measles in India by 2020. BMJ. 2015;350:h900. of pneumococcal, meningococcal, and Haemophilus disease in PMID:25701024 the Middle East and North Africa (MENA) region—current status 6. WHO-recommended standards for surveillance of selected and needs. Vaccine. 2007 Mar 1;25(11):1935–44. PMID:17241707 vaccine-preventable diseases. Geneva: World Health Or- 18. International Coordinating Group on Vaccine Provision for Epi- ganization; 2003. (WHO/V&B/03.01) (http://www.mea- demic Meningitis Control. Global alert and response [Internet]. slesrubellainitiative.org/wp-content/uploads/2013/06/ Geneva: World Health Organization; 2010 (http://www.who. WHO-surveillance-standard.pdf, accessed 19 January 2016). int/csr/disease/meningococcal/icg/en/index.html, accessed 7. Elsaid MF, Flamerzi AA, Bessisso MS, Elshafie SS. Acute bacte- 16 January 2016). rial meningitis in Qatar. Saudi Med J. 2006 Feb;27(2):198–204. 19. MacNeil JR, Bennett N, Farley MM, Harrison LH, Lynfield PMID:16501676 R, Nichols M, et al. Epidemiology of Infant Meningococcal 8. Dash N, Al Khusaiby S, Behlim T, Mohammadi A, Mohammadi Disease in the United States, 2006–2012. Pediatrics. 2015 E, Al Awaidy S. Epidemiology of meningitis in Oman, 2000– Feb;135(2):e305-11. PMID: 25583921 2005. East Mediterr Health J. 2009 Nov-Dec;15(6):1358–64. 20. Castelblanco RL, Lee M, Hasbun R. Epidemiology of bacterial PMID:20218125 meningitis in the USA from 1997 to 2010: a population-based 9. Dash N, Ameen AS, Sheek-Hussein MM, Smego RA Jr. Epide- observational study. Lancet Infect Dis. 2014 Sep;14(9):813–9. miology of meningitis in Al-Ain, United Arab Emirates, 2000– PMID:25104307 2005. Int J Infect Dis. 2007 Jul;11(4):309–12. PMID:16950640 21. von Gottberg A, de Gouveia L, Tempia S, Quan V, Meiring S, von 10. Peltola H. Worldwide Haemophilus influenzae type b disease at Mollendorf C, et al.; GERMS-SA Investigators. Effects of vaccina- the beginning of the 21st century: global analysis of the disease tion on invasive pneumococcal disease in South Africa. N Engl J burden 25 years after the use of the polysaccharide vaccine and Med. 2014 Nov 13;371(20):1889–99. PMID:25386897 a decade after the advent of conjugates. Clin Microbiol Rev. 22. Pneumococcal vaccines WHO position paper—2012. Wkly Epi- 2000 Apr;13(2):302–17. PMID: 10756001 demiol Rec. 2012 Apr 6;87(14):129-44. PMID:24340399 11. Epidemiology and prevention of vaccine preventable diseases, 23. Memish ZA, Shibl AM. Consensus building and recommenda- 13th ed. Atlanta (GA): Centers for Disease Control and Preven- tions based on the available epidemiology of meningococcal tion; 2015 (http//www.cdc.gov/vaccines/puls/pinkbook, ac- disease in Gulf Cooperation Council States. Travel Med Infect cessed 16 January 2016). Dis. 2011 Mar;9(2):60–6. PMID:21345738 12. Shabani IS, Al-Ateeqi W, Abu-Shanab O, El-Sori H, Omar N, 24. Ceyhan M, Anis S, Htun-Myint L, Pawinski R, Soriano-Gabarró Ahmed HF, et al. Childhood meningitis in Kuwait: epide- M, Vyse A. Meningococcal disease in the Middle East and North miology of etiologic agents and the need for pneumococ- Africa: an important public health consideration that requires cal disease prevention. Med Princ Pract. 2006;15(6):431–5. further attention. Int J Infect Dis. 2012 Aug;16(8):e574–82. PMID:17047350 PMID:22647750 13. Tsai C, R. Griffin M, Nuorti P, Grijalva C. Changing epidemiology 25. Howidi M, Muhsin H, Rajah J. The burden of pneumococ- of pneumococcal meningitis after the introduction of pneumo- cal disease in children less than 5 years of age in Abu Dhabi, coccal conjugate vaccine in the United States. Clin Infect Dis. United Arab Emirates. Ann Saudi Med. 2011 Jul-Aug;31(4):356–9. 2008 Jun 1;46(11):1664–72. PMID:18433334 PMID:21808110

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Change in attitudes and knowledge of problem drug use and harm reduction among a community cohort in Kabul, Afghanistan C.S. Todd,1 M.R. Stanekzai, 2A. Nasir,2 K. Fiekert,2 M.G. Orr,3 S.A. Strathdee 4 and D. Vlahov 5

التغــري الــذي طــرأ عــى االجتاهــات واملعــارف املتعلقــة بمشــكلة تعاطــي املخــدرات ّ واحلــدمــن أرضارهــا لــدى إحــدى الفئات املجتمعيــة يف كابول بأفغانســتان كاثرين تود، م. رازا ستانيكزاي، عبد النارص، كاتيا فيكرت، مارك أور، ستيفاين ستاثدي، ديفيد فلوف اخلالصــة:هــذا التقييــم ملــا قبــل ومــا بعــد تطبيــق الربنامــج هيــدف إىل قيــاس التغــريات التــي طــرأت عــى املعــارف واالجتاهــات جتــاه متعاطــي املخــدرات لــدى ممثلــنيعــن املجتمــع يف كابــول بأفغانســتان خــال فــرة مــن فــرات التوســع يف تطبيــق برنامــج ملعاجلــة إدمــان املخــدرات 2009 2007 18 160 واحلــد مــن أرضارهــا. فقــد قامــت عينــة ملئمــة تضــم ًمهنيــا أعمرهــم ســنة فــا فــوق بمــلء اســتبيانات َمقابلــة يف عامــي و . فتبــنيأن اآلراء املؤيــدة جلــودة الربنامــج ولتوفــري الواقــي الذكــري وتقديــم املشــورة واالختبــارات اخلاصــة بالعــدوى وتوزيــع اإلبــر واملحاقــن قــد ازدادت زيــادة ملحوظــة خــال هذيــن العامــني. وكان هنــاك تغــري جوهــري يف مســتوى القبــول )أكثــر مــن % (10 يف 13 ًبيانــا مــن أصــل 38 ، ال ّســيم لــدى الرجــال وأصحــاب املهــن الطبيــة. املتعلقــة بدعــم متعاطــي املخــدرات إجيابيــة إىل حــد كبــري، مــع تغــريات كبــرية يف مواقــف بعــض املجموعــات الســكانية الفرعيــة. ربــا تكــون هنــاك حاجــة إىل مزيــد مــن تثقيــف املجتمــع- عــنطريــق وســائل اإلعــام - وإىل سياســة حكوميــة أكثــر ً متاســكابشــأن املخــدرات، ِّ ز دعــمتعــز املجتمــع ملعاجلــة تعاطــي املخــدرات واحلــد مــن أرضارهــا يف أفغانســتان.

ABSTRACT This pre–post evaluation aimed to measure changes in knowledge and attitudes towards drug users among community representatives in Kabul, Afghanistan, over a period of expansion of harm reduction and drug dependence programming. A convenience sample of 160 professionals aged 18+ years completed interview questionnaires in 2007 and 2009. Views endorsing programme quality and the provision of condoms, infection counselling/testing and needle/syringe distribution increased significantly over the 2-year period. In 13 of 38 statements, there was a substantial (> 10%) change in agreement level, most commonly among men and medical professionals. Attitudes concerning support of drug users remained largely positive, with substantial attitude changes in some subgroups of the population. Further community education through the media and a more cohesive government drug policy may be needed to strengthen community support for harm reduction/drug treatment in Afghanistan.

Évolution des attitudes et des connaissances en matière de toxicomanies et de réduction des effets nocifs au sein d’une cohorte communautaire à Kaboul (Afghanistan)

RÉSUMÉ La présente évaluation pré-post visait à mesurer l’acquisition de connaissances et les changements d’attitudes à l’égard des toxicomanes parmi les représentants d’une communauté à Kaboul (Afghanistan) au cours d’une période d’élargissement des programmes de réduction des effets nocifs et de traitement de la dépendance aux drogues. Un échantillon de commodité de 160 professionnels âgés de plus de 18 ans a rempli des questionnaires dans le cadre d’entretiens en 2007 et en 2009. Les opinions au sujet de l’application de programmes de qualité et de la fourniture de préservatifs, du conseil et du dépistage en matière d’infections, ainsi que de la distribution d’aiguilles/de seringues se sont considérablement améliorées au cours de ces deux années. Dans 13 des 38 déclarations, on a pu noter un changement notable (>10 %) dans le niveau d’acceptation, le plus souvent parmi les hommes et les professionnels de santé. Les attitudes concernant le soutien à apporter aux toxicomanes sont restées positives dans une large mesure, avec des changements d’attitude notables dans certains sous-groupes de la population. Une éducation plus poussée des communautés par le biais des médias et des politiques gouvernementales de lutte contre la drogue plus cohérentes sont nécessaires pour renforcer le soutien communautaire à la réduction des effets nocifs/au traitement des toxicomanies en Afghanistan.

1Department of Obstetrics and Gynaecology, Columbia University and Heilbrunn Department of Population and Family Health, Mailman School of Public Health, New York, United States of America (Correspondence to C. Todd: [email protected]) (Authors' affiliations continued on page192 ) Received: 16/02/15; accepted: 22/12/15

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Introduction we assessed community attitudes and and risk behaviours among a cohort of knowledge about people who inject people who inject drugs. During this pe- Community support is an important drugs (13). The findings highlighted riod, media coverage and programmes component of successful drug depend- some contradictory views; participants for drug users increased substantially, as ence treatment and harm reduction believed that drug use was motivated witnessed by an expansion of harm re- programmes (1–3). Studies among by criminal activity or moral weakness duction programmes (based on needle people who inject drugs indicate that but they also agreed with statements and syringe collection and distribution) perceived lack of support and stigma indicating that drug addiction was a from 3 to 5, an increase of public, no- from the community or family can deter disease and indicated that they would cost drug treatment programmes from drug users from disclosing their HIV be willing to participate in a programme 3 to 6, as well as an increase in the num- status or utilizing harm reduction ser- to help drug users. Only 33% correctly ber of private treatment programmes. vices and can increase their feelings of identified the legal implications of drug The institutional review boards of isolation and propensity towards risky use in Afghanistan. the University of California, San Diego, injecting behaviours (4–6). However, In the context of an increase both Columbia University, and the Ministry few studies have specifically assessed in the rate of problem drug use in the of Public Health of the Islamic Republic community attitudes toward drug use city and in the number of programmes of Afghanistan approved this study. and harm reduction prior to or follow- for drug users in Kabul city, a follow-up ing introduction of harm reduction assessment was carried out to evaluate Participants programmes. Hammett et al. found that changes in public perceptions over time. The eligibility criteria and recruitment knowledge and attitudes regarding harm These data would be used to inform of participants was described in the re- reduction improved between baseline nascent harm reduction and drug de- port of the baseline assessment in 2007 and 18 months post-intervention within pendence treatment programmes so (13). A cross-sectional convenience the context of a community-wide struc- that community relations and media sample of community representatives tural intervention in both China and programming could be modified to best was recruited. Eligible participants were Viet Nam (2). Their assessment used support the public health objectives of professionals (principally shop own- cross-sectional sampling waves at each these programmes. The specific objec- ers/workers, medical professionals and time point, rather than longitudinal data tive of this study was to assess changes in government officials) aged 18 years or from the same individuals, thus limiting community knowledge of and attitudes more and residing in Kabul city. At en- the ability of the study to attribute the towards problem drug use and harm rolment during the baseline assessment, effects to the intervention. reduction and treatment programming participants provided an address and In Afghanistan, estimates indicate among a community sample in Kabul, telephone number which were used to that problem drug use increased be- Afghanistan. contact them for the follow-up assess- tween 2005 and 2009 and that drug us- ment. Of the 210 participants recruited ers, particularly those injecting opiates, at baseline, 160 completed the follow- tend to be concentrated in urban areas Methods up questionnaire. (7,8). The subsequent donor response Data collection since 2007 has been to increase or Study design and setting expand the number of drug depend- This paper reports a pre- and post-inter- Questionnaire ence treatment and harm reduction vention assessment of knowledge and at- The questionnaire instrument used for programmes and services (9,10). Nev- titudes among a sample of community the baseline and follow-up data col- ertheless, use of intoxicants is forbidden representatives in Kabul, the capital of lection has been described previously in , and the current laws regarding Afghanistan. Kabul is divided into 17 (13). Briefly, this instrument collected drug use reflect this paradox, in that municipal districts and has an estimated information regarding attitudes toward a first offence is eligible for treatment metropolitan population of 5 million. drug use and appropriate treatment and while repeat offenders are imprisoned In the last decade, the population has also assessed knowledge of current drug (11). In a 2006 qualitative assessment increased considerably due to returning laws and availability of treatment. In of people who inject drugs in Kabul, refugees and to internal displacement baseline and follow-up questionnaires, many participants reported open secondary to conflict and other events the same knowledge and attitude ques- condemnation by various community (14). This assessment of community tions were used to ensure consistency. members and a sense of isolation and attitudes was part of a larger study con- The long interval between completion fear that coloured all interactions with ducted from June 2006 to November of the two questionnaires likely mini- the community at large (12). In 2007, 2009 evaluating harm reduction use mized any bias secondary to repeated

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testing. Prior to baseline data collection, Subsequent analysis considered only Changes in perceptions the draft instrument was pre-tested for participants available at both study towards drug users in content and face validity among 20 visits. Assessment of the change in Afghanistan volunteers of different sexes, locations awareness and knowledge of drug use Changes in perceptions and experienc- within Kabul city and professions. The over time was assessed with McNemar es towards drug users between baseline study manager and principal investiga- chi-squared and exact tests and paired and follow-up for the 160 participants tor assessed the accuracy of the final t-tests, as appropriate. who completed both assessments are changes to the questionnaire through Attitudes toward drug use and displayed in Table 1. At follow-up, back-translation. treatment were measured with Lik- significantly fewer individuals had en- countered a drug user in the last 2 years Study activities ert scales, with differences in level of agreement between baseline and (69.4% compared with 84.4% at base- An interim analysis of the cohort data follow-up analysed using Wilcoxon line, P < 0.01). Tobacco was now per- from the main study of drug users was sign-rank test. Statements with less ceived to be the most commonly used performed in February 2009, 18 months than 20% of participants differing illicit substance (58.1% versus 16.9% at following the initiation of enrolment. from the majority were considered to baseline, P < 0.01) whereas marijuana/ A results meeting was convened and have consensus. Consistent with the hashish were perceived as less common attended by key government officials, baseline analysis, the 80% mark was (19.4% versus 45.6% at baseline, P < civil society organization stakeholders selected to highlight the most contro- 0.01). Perceptions regarding those at and available community participants. versial positions (13,15,16). For state- greatest risk for initiating drug use also This meeting included a presentation ments demonstrating > 10% change changed, as prisoners and those work- of the preliminary study results, a panel in consensus, sociodemographic and ing in heroin processing facilities were discussion with drug users and govern- experiential (e.g. having a family mem- perceived to be at greater risk than 2 ment officials, and speeches by an -offi ber who was a drug user) factors were years earlier. All perceived reasons for cial from the Ministry of Public Health analysed with ordinal logistic regres- initiating drug use (multiple answers and a member of Parliament. Local sion to determine associations with allowed) were assessed. At follow-up, media covered the event and portions changes in attitudes. significantly more participants than at of it were televised, potentially reach- baseline believed that peer pressure and ing community participants unable to sadness over loss of home and family attend. Results were reasons why people initiated drug In the month prior to the results use. Perceived harms associated with meeting, the researchers contacted the Of 210 participants at baseline, 160 drug use (multiple answers permitted) participants from the baseline assess- (72.7%) completed the follow-up visit, showed that significantly fewer partici- ment of community attitudes; those of whom 39 (24.4%) attended the re- pants saw health-related problems (e.g. contacted received a written invitation sults meeting. Participants retained in overdose, withdrawal and infections) to the meeting. Following the results the study were more likely to be govern- as the greatest harms associated with meeting in April 2009, study staff ment (P = 0.03) and university officials drug use, while family disapproval and contacted participants and scheduled (P < 0.01) than those who dropped imprisonment increased as perceived interviews at a site convenient to the out. Those who had lived outside Af- harms. participant starting in July 2009. Study ghanistan within 5 years of enrolment staff confirmed the identity of the par- were marginally more likely to complete Knowledge and perceptions ticipant via the assigned study number the follow-up interview (79% versus regarding appropriate and then administered the follow-up 66%, P = 0.07), while younger partici- response to drug use questionnaire. Participants were not pants (mean age at baseline 33.6 years At follow-up, fewer participants (25.6% compensated financially for their par- versus 37.6 years, P = 0.02), medical versus 33.3% at baseline, P = 0.01) ticipation. professionals (P < 0.01) and the police stated that they knew the laws regard- (P = 0.01) were less likely to complete ing drug use in Afghanistan. Of those Analysis both assessments. During the interval claiming knowledge, only 41.0% (n = Differences in sociodemographic char- between baseline and follow-up, par- 22) correctly described that treatment acteristics between participants avail- ticipants experienced some changes in was provided for the first offence (if able for follow-up visits and those lost employment status, with 6% gaining available) and that those with subse- to follow-up were compared using the employment and 13% becoming unem- quent offences were incarcerated chi-squared and t-test, as appropriate. ployed (P = 0.04). (open-ended question). Participants

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Table 1 Changes in perceptions and experiences regarding drug use between baseline and follow-up assessments among community representatives (n = 160) in Kabul, Afghanistan Variable Baseline Follow-up P-value a No. % No. % Encountered a drug user in last 2 years 135 84.4 111 69.4 < 0.01 Have a drug user in the family 17 10.6 13 8.1 0.54 Most common drug used in Afghanistan Tobacco 27 16.9 93 58.1 < 0.01 Marijuana/hashish 73 45.6 31 19.4 < 0.01 Opium/heroin 44 27.5 27 16.9 0.01 Alcohol 13 8.0 9 5.6 0.39 Group at greatest risk for drug use Unemployed 139 86.9 82 51.3 < 0.01 Prisoners 2 1.3 27 16.9 < 0.01 Heroin processing facility workers 5 3.1 14 8.8 0.06 Former/current soldiers 2 1.3 13 8.0 < 0.01 Street children 11 6.9 17 10.6 0.34 Most common perceived reason for initiating drug use (multiple responses allowed) Peer pressure 48 30.0 85 53.1 < 0.01 Frustration over unemployment 105 65.6 82 51.3 < 0.01 Sadness over loss of family/home 39 24.4 69 43.1 < 0.01 Enjoyment of the drug’s effect 59 36.9 42 26.3 0.04 Improve work output 25 15.6 33 20.6 0.23 Perceived greatest harms associated with drug use Family disapproval 80 50.0 135 84.4 < 0.01 Imprisonment 24 15.0 102 63.8 < 0.01 Overdose 77 48.1 53 33.1 < 0.01 Infections (e.g. hepatitis) 49 30.6 22 13.8 < 0.01 Withdrawal 76 47.5 20 12.5 < 0.01 Violence from dealers/other users 22 13.8 17 10.6 0.47 Types of treatment available for drug dependency (n = 132) Detoxification 12 9.1 21 15.9 0.09 Inpatient hospital stay 124 93.9 125 94.7 1.00 Medicines from pharmacy 32 24.2 12 9.1 < 0.01 Counselling programmes 42 31.8 85 64.4 < 0.01 Religious instruction 32 24.2 28 21.2 0.53 Measures perceived as most important to reduce harm to drug users Increased availability of dependency treatment 146 91.3 141 88.1 0.47 Improved quality of dependency treatment 55 34.4 74 46.3 0.02 Provision of vocational training 129 80.6 127 79.4 0.77 Provision of condoms and counselling and testing for 18 11.3 72 45.0 < 0.01 infections Increased imprisonment/sentences for drug users 10 6.3 16 10.0 0.29 Increased number of police in areas where drug users 22 13.8 15 9.4 0.26 congregate Provision of needles and syringes to those who inject 18 11.3 31 19.4 0.03 Increased Islamic teaching about drug use 83 51.9 68 42.5 0.08

aMcNemar or exact McNemar chi-squared test.

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were similarly asked about the most of the 11 statements without con- in Viet Nam (1,2,10). However, despite appropriate response towards drug use sensus, 6 did not have consensus at positive changes in attitudes to the in Afghanistan, to which a variety of baseline. However, 17 statements had value of needle and syringe collection responses were elicited and categorized statistically significant changes in indi- and distribution programmes and to by content. Participants largely favoured vidual scores between baseline and fol- counselling and testing, less than half of medical treatment (50.2% versus 49.5% low-up measures and 13 had substantial participants supported these measures. at baseline), with lifestyle modification (> 10%) changes in overall levels of The smaller number of participants at (25.1% versus 25.2%) and counselling/ agreement. Factors significantly associ- follow-up reporting having encoun- supportive care (20.0% versus 16.4%) ated with > 10% change are shown in tered a drug user may have influenced also mentioned, with little change from Table 3. Male participants and medical these results. baseline levels that were reported in professionals were the groups most Replies regarding the most ap- an earlier paper (13). Fewer respond- likely to have significant changes in propriate response to drug use were ents (4.7% versus 16.4% at baseline) levels of agreement over time, while consistent over time; the continued advocated punitive measures as the ap- loss of employment, attendance at the emphasis on medical treatment is reas- propriate response to drug use. results meeting and age were not associ- suring and supports positive changes in ated with changes between baseline and the perceived benefits of drug treatment Awareness and attitudes follow-up for any statement. and harm reduction, potentially due toward harm reduction and to the greater number and visibility of addiction treatment such programmes in the community Most participants remained aware that Discussion during the study period. The greatest drug treatment programmes were avail- perceived harms of drug use changed able in Afghanistan (88.6% at baseline, The key findings of the study include from health concerns to loss of social 87.5% at follow-up, P = 0.30). At follow- increasingly positive perceptions of position, including family disapproval up, participants had greater familiarity programmes for drug users (counsel- and imprisonment. This change may with counselling programmes (64.4% ling and HIV testing programmes and result from the increasing stress of versus 31.8% at baseline, P < 0.01) and needle/syringe collection and distribu- burgeoning urban populations and re- detoxification programmes (15.9% tion schemes), and an increased belief source scarcity on the family unit, the versus 9.1% at baseline, P < 0.09), while in the association of drug-related harm chief social support structure in Afghan less knowledge of obtaining medicines with disintegration of family support. society (17,18). Keeping a drug user as a pharmacy for treatment (24.2% Both positive and negative shifts in over- within the family unit likely equates versus 9.1% at baseline, P < 0.01) (Ta- all attitudes over time among several to survival in the perceptions of many ble 1). When asked about which ap- groups of individuals were also detected people, and removal of the drug user is proaches were the most important to at the end of the study period, although thus perceived as a greater risk than ill reduce harm to drug users, factors that there was a reduction in self-professed health. More participants believed that were mentioned significantly more fre- knowledge of current drug use laws. sadness over loss of home and family or quently than at baseline were: improv- Increasing the availability of drug imprisonment were reasons for initiat- ing drug treatment quality, providing treatment and providing vocational ing drug use, and this change may also condoms and counselling and testing training remained the most endorsed reflect fears surrounding displacement for infections, and providing needles measures to aid drug users. The per- from the family unit. Drug use in pris- and syringes to people who inject drugs ceived value of needle and syringe col- ons has been documented in various (Table 1). lection and distribution programmes, settings, including countries bordering of condom distribution and voluntary Afghanistan, and knowledge of this has Attitude scale results counselling and HIV testing pro- potentially permeated into the commu- Participants were read 38 statements grammes and of improved treatment nity (19–22). Peer pressure increased for which they indicated a level of agree- programme quality increased over time. as a perceived reason to initiate drug ment, measured by a Likert scale. Table This change may reflect the increased use, perhaps due to media coverage 2 lists all the statements, the levels of numbers of programmes and the in- of the issue or to respondents’ direct consensus at baseline and follow-up, creased media coverage of drug use in experiences (23,24). and the significance of changes from urban Afghan settings, as well as pro- One-third of attitude statements baseline. At follow-up, consensus gramme efforts to educate and involve showed a substantial overall change in (> 80%) or approaching consensus surrounding communities in their ac- respondents’ level of agreement, with 4 (> 70%) was present for 27 statements; tivities, similar to experiences reported statements demonstrating potentially

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Table 2 Statements conveying attitude towards drug use and harm reduction with group level of consensus at follow-up visit and differences between baseline and follow-up measures among community representatives (n = 160) in Kabul, Afghanistan, 2009 Statement % agreeing P-valueb Baseline Follow-up Drug use is increasing in Afghanistan 96.2 96.3 0.21 Accessibility of opium and dealing drugs in Afghan society has increased 92.4 98.1 0.01 Injecting drug use is increasing in Afghanistan 73.8 80.0 0.06 Afghan culture is becoming more tolerant of drug usea 14.8 38.1 < 0.01 Drug use in Afghanistan is directly related to the large amounts of opium currently grown 75.2 71.3 0.23 The level of community awareness about drug use in Afghanistan is adequate to address the problema 21.9 52.5 < 0.01 Drug addiction is motivated by criminal activity or moral weakness 84.8 93.1 0.05 Drug addiction is a disease 88.6 81.9 Drug users are a danger to decent people 93.8 88.7 0.98 It is acceptable for families to cease relations with family members who use drugs 43.3 47.5 0.33 There are no circumstances under which drug use is acceptable 84.3 93.1 0.02 Addiction causes people to turn to criminal activity to pay for drugs 96.7 97.5 0.70 Injecting drug users increase their risk of health problems by removing their blood and replacing it with drugs 90.0 83.8 0.18 Injecting drugs is worse than other kinds of drug use 80.4 88.8 0.04 Injecting drugs is advised to drug users by doctors to reduce the dependence on drugs a 26.2 39.4 < 0.01 Injecting drug use causes health problems like jaundice 82.5 82.4 0.65 The greatest threat of drug users in society is the disintegration of the family 89.5 93.1 0.86 Consumption of all intoxicating drugs is prohibited by Islam 96.2 95.0 0.32 Intoxicating substance use should be allowed in extreme cases of physical or psychological pain a 56.7 13.8 < 0.01 Joblessness increases the risk someone will start using drugs 95.2 98.1 0.21 Women are more likely to use drugs as they are more easily influenced to pursue the wrong behaviour a 24.8 59.4 < 0.01 Afghan society and Islam both regard drug use to be a sin 96.7 95.6 0.75 Only religious leaders should help drug users through intensive prayer sessionsa 55.2 37.5 0.01 Drug treatment centres should be established to help those with addiction 95.2 97.5 0.32 It is appropriate to use zakat money for the establishment of drug addiction treatmenta 83.3 66.3 < 0.01 Only families are obligated to get help and treatment for family members who use drugs 24.8 32.5 0.05 Only the government is obligated to provide treatment services for people who use drugsa 49.5 31.3 < 0.01 Only religious leaders should decide what treatment is most appropriate for drug users in Afghanistan 12.4 17.5 0.07 Eradication of poppy crops alone will be sufficient to control opium use in Afghanistan 49.5 56.3 0.22 Community messages stating “Say no to drugs” alone will be sufficient to prevent drug and alcohol use in Afghanistana 16.7 46.9 < 0.01 The entire community should be educated about the harms of drug use to adequately prevent an increase drug use 94.3 96.3 0.44 Religious leaders and teachers should use their influence to increase community awareness for drug use preventiona 87.2 97.5 < 0.01

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Table 2 Statements conveying attitude towards drug use and harm reduction with group level of consensus at follow-up visit and differences between baseline and follow-up measures among community representatives (n = 160) in Kabul, Afghanistan, 2009 (concluded) Statement % agreeing P-valueb Baseline Follow-up Police should be a priority group to receive educational programming about how to behave towards drug usersa 83.8 97.5 < 0.01 I would be comfortable if a harm reduction centre opened near my home 75.2 85.0 0.09 I would be comfortable participating in a programme to help drug users 94.3 86.9 < 0.01 I am comfortable speaking with or praying next to drug usersa 64.8 76.9 0.09 I approve if any member of my family were to work with a programme to help drug usersa 7 7. 1 88.8 0.11 I would be willing to hire or work with a former drug user 80.0 84.4 0.43

aChange of more than 10% in level of overall consensus for statement; bSign-rank test.

detrimental trends. Exposing partici- treatment centres with zakat—the tith- media. This issue would benefit from pants to the preliminary results of harm ing of income for charitable causes in inquiry in future assessments because reduction programmes—as recom- Islam—and this may reflect increased pharmaceutical intoxicant misuse is a mended by a community assessment awareness and negative community common and under-recognized prob- in Viet Nam and China—had no perceptions toward these private profit- lem in Afghanistan (26). measurable impact on community rep- based drug treatment clinics, potentially Finally, the increased perception resentatives’ attitudes in Kabul 2( ). Low translating to negative perceptions of all that women were particularly at risk for attendance at the results meetings may drug treatment programmes. Negative drug misuse may reflect some loss of have hindered sufficient dissemination views of using zakat for this purpose ground for women’s rights in Afghani- of the programme findings to demon- were more likely among shop owners, stan. An article in the press reported strate an effect. There was increased who may experience begging or con- approval of an edict officially describing agreement among respondents that cern for theft from drugs users which women as second-class citizens (27), a community awareness of drug use was diminish their charitable feelings to- belief increasingly espoused in the me- adequate to address problem drug use, wards them. dia and potentially accounting for the thus reflecting the impact of expanded The respondents in this study shift in attitude, which was significant community-based and media efforts to showed decreased support towards the among male participants, during the publicize drug use in Afghanistan dur- use of intoxicants for patients in extreme study period. ing the study period (10). pain. This is concerning, although it On a positive note, over time, par- Our respondents had an increased may reflect differences in interpretation ticipants reported increasing comfort odds of agreement with the statement of the question, which did not specify interacting with drug users. However, that injecting drug use was recommend- whether “intoxicating substances” in- the level of comfort significantly de- ed by health professionals as a way to cluded pharmaceutical opiates or other creased for shop owners, as mentioned reduce drug dependence. This may re- medicines. Respondents may have as- before. High levels of agreement per- flect misperceptions about appropriate sumed that the question referred only sisted for statements reflecting comfort drug treatment. However, during the to heroin and other opiates. Significant with harm reduction, willingness to hire study period, many private addiction positive changes in responses to this former drug users as employees and “treatment” clinics became available, us- statement occurred for those with a willingness for themselves or a family ing pharmaceutical narcotics to replace family member who was a drug user, member to participate in programmes illicit opioids and with a short-term oral potentially reflecting their greater un- to help drug users. This change is course with a tapered dose provided at derstanding of drug dependency and its somewhat surprising given the reduced discharge. This regimen likely has a high predisposing conditions. Participants amount of contact with drug users over failure rate and needs repeated courses with higher levels of education were time, but may be attributable to media of treatment, thus ensuring sustained more likely to change towards more coverage of the growing problem of profit for clinics 25( ). Our participants negative attitudes, possibly reflecting drug use and the positive profiles of had a reduced level of agreement that trends toward conservative ideals based some drug treatment centres within the it was appropriate to establish drug on exposure to the written and visual media and community (10).

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Table 3 Variables associated with change in agreement with selected attitude statementsa about drug use and harm reduction between baseline and follow-up measures by ordinal logistic regression among community representatives (n = 160) in Kabul, Afghanistan, 2009 Attitude statement/associated variables Mean score OR 95% CI Baseline Follow-up Afghan culture is becoming more tolerant of drug use No significant correlates – – – – The level of community awareness about drug use in Afghanistan is adequate to address the problem Marital status (married) 2.01 3.11 2.16 1.06–4.42 Education (any secondary education) 1.89 3.02 3.35 1.17–9.57 Injecting drugs is advised to drug users by doctors to reduce the dependence on drugs Occupation (medical professional) 2.40 3.37 2.23 1.11–4.47 Intoxicating substance use should be allowed in extreme cases of physical or psychological pain Education (any secondary education) 2.68 1.57 0.32 0.11–0.92 Education (university education or higher) 2.88 1.67 0.36 0.13–0.97 Exposure (have family member who uses drugs) 2.33 2.17 3.49 1.03–11.8 Women are more likely to use drugs as they are more easily influenced to pursue the wrong behaviour Sex (male) 2.54 3.58 2.33 1.19–4.57 Only religious leaders should help drug users through intensive prayer sessions Sex (male) 3.33 2.44 0.27 0.14–0.53 Travel experience (lived outside Afghanistan in the last 5 years) 2.88 2.97 2.13 1.05–4.34 Occupation (shop owner/worker) 2.92 3.36 2.52 1.16–5.47 Occupation (medical professional) 2.77 2.77 2.23 1.13–4.41 It is appropriate to use zakat money for the establishment of drug addiction treatment Occupation (shop owner/worker) 3.92 3.00 4.47 1.95–10.3 Only the government is obligated to provide treatment services for people who use drug Sex (male) 3.34 2.35 0.42 0.21–0.85 Occupation (medical professional) 2.57 1.83 2.79 1.38–5.64 Community messages stating “Say no to drugs” alone will be sufficient to prevent drug and alcohol use in Afghanistan Sex (male) 1.93 2.79 2.98 1.33–6.66 Marital status (married) 2.03 2.81 2.38 1.04–5.43 Religious leaders and teachers should use their influence to increase community awareness for drug use prevention Sex (male) 4.30 4.24 5.02 1.30–19.45 Police should be a priority group to receive educational programming about how to behave towards drug users Occupation (government official) 3.87 4.65 3.22 1.33–7.82 I am comfortable speaking with or praying next to drug users Occupation (shop owner/worker) 3.80 3.60 0.36 0.14–0.91 I approve if any member of my family were to work with a programme to help drug users No significant correlates – – – –

aStatements selected are those with > 10% change in consensus between baseline and follow-up measures. OR = odds ratio; CI = confidence interval.

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One further attitude statement mer- The follow-up questionnaire did not of drug users. A programme in the its mention, as significant differences include questions eliciting specific United States of America demonstrated were noted among 3 groups. Those sources for information that may have increased community knowledge who had lived outside Afghanistan were altered knowledge and attitude over and participation in programmes for more likely to agree that only religious time; the increased media attention on drug users after members of the com- leaders should help drug users via in- problem drug use and community out- munity had viewed a play consisting tensive prayer sessions and this may be reach by harm reduction and treatment of vignettes of drug users’ life stories due to limited awareness of drug user programmes may have had differential (28). Furthermore, drug treatment and programmes in Kabul. It is surprising that effects. Finally, quantitative data do not harm reduction programmes could medical professionals also had a higher provide sufficient insight into reasons engage communities more widely or odds of endorsing this statement, as the for attitude changes, leaving much room frequently, although migration within mean attitude score did not change for for conjecture. Further qualitative work communities, limited programme staff this group. This lack of change may come is indicated to better delineate com- and funding, and security limitations from the high failure rates associated with munity perceptions surrounding drug may make this approach untenable drug treatment, fostering the opinion misuse, harm reduction and treatment. in Afghanistan, despite its success in that spiritual therapy may be no worse other settings 1( ,2). Finally, political than other treatment modalities (28). will should be exercised to unify the Shop owners and workers, who may have Conclusions and disparate policy positions on drug use a more conservative outlook than those recommendations and treatment, and in particular those in other professions, had higher odds on harm reduction, between different of agreement. By contrast, male partici- In conclusion, the major finding from sectors in the Afghan government (25). pants, who have greater access to media the study is that drug dependency in and may travel freely, were less likely to Kabul continues to be perceived by endorse this view than were females, pos- community representatives as a disease Acknowledgements sibly reflecting their greater awareness of for which treatment and vocational programme options and successes that training are the preferred response. We thank harm reduction programme did not involve religious instruction. Perceptions of the worst harm associ- colleagues of Médecins du Monde, Some limitations to the study in- ated with drug use and the reasons for Nejat Center and the Organization of clude the relatively low follow-up rate, initiating drug use changed during the Technical Cooperation for Commu- which may have limited our ability to study period, as did the context of drug nity Development for their collabora- detect some associations, notably for use and treatment in Kabul. Several tive efforts. We appreciate the support several professional cadres, and may trends in negative attitudes emerged of the Ministries of Counter-Narcotics have inadvertently included individuals that indicate a need for focused media- and Public Health. We thank the par- whose views did not reflect the major- based messages. Thus, the first recom- ticipants for their time, input and trust. ity of original participants. Concerted mendation emerging from the data is to Funding: This study was funded by a effort was made to locate the original address key negative attitudes measured Clinical Scientist Development Award participants, although turnover in the within media and community-based from the Doris Duke Charitable Foun- study staff during the study period may messaging. One promising strategy is dation. have compromised these attempts. drama portraying the lived experience Competing interests: None declared.

References

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7. Afghanistan drug abuse survey. Kabul, Afghanistan: United Na- tional prison survey in England and Wales. Addiction. 2002 tions Office on Drugs and Crime; 2005. Dec;97(12):1551–60. PMID:12472639 8. Drug use in Afghanistan: 2009 survey. Executive summary. Ka- 20. Wood E, Lim R, Kerr T. Initiation of opiate addiction in a bul, Afghanistan: United Nations Office on Drugs and Crime; Canadian prison: a case report. Harm Reduct J. 2006;3:11. 2010. PMID:16542427 9. Saif-ur-Rehman, Rasoul MZ, Wodak A, Claeson M, Friedman 21. Zamani S, Farnia M, Torknejad A, Alaei BA, Gholizadeh M, Kas- J, Sayed GD. Responding to HIV in Afghanistan. Lancet. 2007 raee F, et al. Patterns of drug use and HIV-related risk behaviors Dec 22;370(9605):2167–9. PMID:18156038 among incarcerated people in a prison in Iran. J Urban Health. 10. Maguet O, Majeed M. Implementing harm reduction for 2010 Jul;87(4):603–16. PMID:20390391 heroin users in Afghanistan, the worldwide opium supplier. Int 22. Kazi AM, Shah SA, Jenkins CA, Shepherd BE, Vermund SH. Risk J Drug Policy. 2010 Mar;21(2):119–21. PMID:20171864 factors and prevalence of tuberculosis, human immunode- 11. Todd CS, Safi N, Strathdee SA. Drug use and harm reduction in ficiency virus, syphilis, hepatitis B virus, and hepatitis C virus Afghanistan. Harm Reduct J. 2005 Sep 7;2:13. PMID:16146577 among prisoners in Pakistan. Int J Infect Dis. 2010 Sep;14 Suppl 3:e60–6. PMID:20189863 12. Todd CS, Stibich MA, Stanekzai MR, Rasuli MZ, Bayan S, Wardak SR, et al. A qualitative assessment of injection drug 23. Rubin AJ, Rahimi S. Few treatment options for Afghans as use and harm reduction programmes in Kabul, Afghani- drug use rises. The New York Times. 2011 Aug 27 (http:// stan: 2006–2007. Int J Drug Policy. 2009 Mar;20(2):111–20. www.nytimes.com/2011/08/28/world/asia/28kabul. PMID:18207381 html?pagewanted=all, accessed 29 January 2016). 13. Stanekzai MR, Todd CS, Orr MG, Bayan S, Rasuli MZ, Wardak 24. Daneshmandan N, Narenjiha H, Tehrani K, Assari S, Khoddami- SR, et al. Baseline assessment of community knowledge and at- Vishteh HR. Initiation to the first drug use among substance-de- titudes toward drug use and harm reduction in Kabul, Afghani- pendent persons in Iran. Subst Use Misuse. 2011;46(9):1124–41. stan. Drug Alcohol Rev. 2012 Jun;31(4):451–60. PMID:21919980 PMID:21345165 14. Humanitarian update: Afghanistan-December 2010. Kabul, 25. Todd CS, Macdonald D, Khoshnood K, Mansoor GF, Eggerman Afghanistan: United Nations Office for the Coordination of M, Panter-Brick C. Opiate use, treatment, and harm reduction Humanitarian Affairs; 2011. in Afghanistan: recent changes and future directions. Int J Drug Policy. 2012 Sep;23(5):341–5. PMID:22717389 15. Raine S. Defining the Bobath concept using the Delphi tech- nique. Physiother Res Int. 2006 Mar;11(1):4–13. PMID:16594311 26. Macdonald DS. Briefing paper series: Afghanistan’s hidden drug problem: the misuse of psychotropics. Kabul, Afghani- 16. Whitehead D. An international Delphi study examining health stan: Afghanistan Research and Evaluation Unit; 2008. promotion and health education in nursing practice, ed- ucation and policy. J Clin Nurs. 2008 Apr;17(7):891–900. 27. Hamid Karzai under fire on Afghan women’s rights. The Tel- PMID:18321288 egraph. 2012 8 Mar (http://www.telegraph.co.uk/news/ worldnews/asia/afghanistan/9130508/Hamid-Karzai-under- 17. Panter-Brick C, Goodman A, Tol W, Eggerman M. Mental fire-on-Afghan-womens-rights.html, accessed 29 January health and childhood adversities: a longitudinal study in Ka- 2016). bul, Afghanistan. J Am Acad Child Adolesc Psychiatry. 2011 Apr;50(4):349–63. PMID:21421175 28. Joe GW, Simpson DD, Broome KM. Effects of readiness for drug abuse treatment on client retention and assessment of 18. Dupree NH. The family during crisis in Afghanistan. J Comp process. Addiction. 1998 Aug;93(8):1177–90. PMID:9813899 Fam Stud. 2004;35(2):311–31. 19. Boys A, Farrell M, Bebbington P, Brugha T, Coid J, Jenkins R, et al. Drug use and initiation in prison: results from a na-

Authors' affiliations continued from page183

2Health Protection and Research Organization, Kabul, Afghanistan. 3Heilbrunn Department of Population and Family Health, Mailman School of Public Health, New York, United States of America. 4Centre for Urban Epidemiologic Studies, The New York Academy of Medicine, New York, United States of America. 5Division of Global Public Health, University of California San Diego School of Medicine, La Jolla, California, United States of America.

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Accuracy of the VITEK® 2 system for a rapid and direct identification and susceptibility testing of Gram- negative rods and Gram-positive cocci in blood samples N.A. Nimer,1 R.J. Al-Saa’da 2 and O. Abuelaish 3

VITEK® 2 دقــة نظــام لالســتعراف الرسيــع واملبــارش عــى العصيــات ســلبية اجلــرام واملكــورات إجيابيــة اجلــرام يف عينــات الــدم واختبــار حساســيتها نبيل عوين النمر، رائدة جال السعايدة، عمر أبو العيش اخلالصــة:تــم حتديــد أداء نظــام VITEK® 2 للســتعراف الرسيــع املبــارش عــى اجلراثيــم املســؤولة عــن عــداوى الــدم واختبــار حساســيتها 74 166 لألدويــة. وقــد شــملت َاملســتفردات املدروســة مسـ�تفردة لعصيـ�ات سـ�لبية اجلـ�رام و مســتفردة ملكــورات إجيابيــة اجلــرام مــن مــرىض داخليــني. وأخــذت عينــات أحاديــة اجلرثــوم - معاجلــة بطريقــة خاصــة - مــن قواريــر َمســتنبتات الــدم اإلجيابيــة، ِّولقحــت مبــارشة يف نظــام VITEK® 2 ، وقورنــت النتائــج مــع تلــك املأخــوذة مــن بطاقــات ملقحــة بمســتعلقات جرثوميــة معــ َّ ة.ري باملقارنــة مــع الطريقــة املعياريــة تــم االســتعراف الصحيــح عــى % 95.8مــن العصيــات ســلبية اجلــرام بواســطةVITEK® 2، وكان مســتوى التوافــق اإلجــايل بــني الطريقتــني يف اختبــار احلساســية %92 وبالنســبة للجراثيــم إجيابيــة اجلــرام تــم االســتعراف الصحيــح عــى %89.2 بواســطة VITEK®، 2 وأظهــر اختبــار احلساســية ًتوافقــا إج ًاليــا بمعــدل %91.3. تشــري هــذه النتائــج إىل أن بطاقــات VITEK® 2 التــي َّتلقــح بســوائل مأخــوذة مبــارشة مــن قواريــر مســتنبتات الــدم اإلجيابيــة تعتــرب مناســبة للســتعراف الرسيــع عــى العصيــات ســلبية اجلــرام واملكــورات إجيابيــة اجلــرام والختبــار حساســيتها.

ABSTRACT The performance of the VITEK® 2 system for direct rapid identification and antimicrobial susceptibility testing of the bacteria responsible for blood infections was determined. The isolates studied included 166 Gram-negative rods and 74 Gram-positive cocci from inpatients. Specially treated monomicrobial samples from positive blood culture bottles were directly inoculated into the VITEK 2 system and the results were compared with those from cards inoculated with standardized bacterial suspensions. Compared with the standard method, 95.8% of Gram-negative rods were correctly identified by VITEK 2 and the overall level of agreement between the two methods in susceptibility testing was 92.0%. For Gram-positive bacteria, 89.2% were correctly identified by VITEK 2 and susceptibility testing revealed an overall agreement rate of 91.3%. These results suggest that VITEK 2 cards inoculated with fluids sampled directly from positive blood culture bottles are suitable for speedy identification and susceptibility testing of Gram-negative bacilli and Gram-positive cocci.

Précision du système VITEK® 2 pour une identification et un test de sensibilité directs et rapides des bâtonnets à gram négatif et des cocci à gram positif dans des échantillons sanguins

RÉSUMÉ La performance du système VITEK® 2 pour une identification et un test de sensibilité aux antimicrobiens rapides et directs des bactéries responsables d’infections sanguines a été mesurée. Les isolats étudiés concernaient 166 bâtonnets à gram négatif et 74 cocci à gram positif prélevés sur des patients hospitalisés. Des échantillons monomicrobiens issus de flacons d’hémoculture positifs ayant été soumis à un traitement spécial ont été directement inoculés dans le système VITEK 2 et les résultats ont été comparés avec ceux issus de cartes inoculées à l’aide de suspensions bactériennes standards. Par comparaison avec la méthode standard, 95,8 % des bâtonnets à gram négatif ont été correctement identifiés par VITEK 2 et le niveau de concordance global entre les deux méthodes en matière de test de sensibilité était de 92,0 %. Pour les bactéries à gram positif, 89,2 % ont été correctement identifiées par VITEK 2 et le test de sensibilité a révélé un taux de concordance de 91,3 %. Ces résultats suggèrent que les cartes VITEK 2 inoculées à l’aide de liquides prélevés directement dans des flacons d’hémoculture positifs sont adaptées à une identification et à un test de sensibilité rapides des bacilles à gram négatif et des cocci à gram positif.

1Faculty of Pharmacy, Philadelphia University, Amman, Jordan (Correspondence to N.A. Nimer: [email protected]). 2Princess Iman Research and Laboratory Sciences Centre, Royal Medical Services, Amman, Jordan. 3King Hussein Medical Center, Royal Medical Services, Amman, Jordan. Received: 03/10/15; accepted: 20/01/16

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Introduction used for the detection and identifica- about the performance of the system tion of microorganisms in blood. The for both identification and susceptibility Bacteraemia is an invasion of the blood- conventional method commonly used testing. In the present study in a labo- stream by viable bacteria that can devel- in clinical laboratories involves inocula- ratory in Jordan, both methodologies op into a serious and deadly infection. tion onto agar media and overnight were applied for the identification and For critically ill patients, bloodstream incubation of fluids from blood cul- susceptibility testing of Gram-negative infections are a major cause of mor- ture bottles, followed by recovery of a rods and Gram-positive cocci and the bidity and mortality despite significant satisfactory bacterial inoculum size to results were compared to evaluate the advances in supportive care and the prepare standard suspensions for identi- performance of the VITEK 2 system. availability of effective antimicrobial fication (biochemical or immunological therapy (1,2). The bloodstream can be tests) and antimicrobial susceptibility infected by microorganisms via various testing (8). However, this method is Methods channels, such as surgical and dental time-consuming as it requires 48–72 procedures, teeth brushing, insertions h (more for slow-growing bacteria) for This study was carried out using bacte- of catheters, urinary tract or gastroin- the results to be obtained, including rial isolates collected from January to testinal infections and intravenous drug 4–24 h of incubation time for blood December 2012 from specimens at the use (3,4). cultures and an additional 24–48 h for Princess Iman Research and Laboratory Sciences Centre of the Royal Medical Different types of bacteria are re- biochemical or immunological tests for Services in Amman, Jordan. sponsible for bloodstream infections. identification and susceptibility testing ( ). These delays have prompted the Gram-negative bacteria were common 8 Detection of microorganisms in the 1970s, especially in hospitalized development of several automated and in blood samples patients, but currently Gram-positive rapid identification and susceptibility testing systems that are used by some The presence of microorganisms in bacteria are the predominant causative blood samples from hospitalized pa- agents (5). Gram-negative bacteria that clinical laboratories. These include the ® tients was detected using the BacT/ are frequently associated with blood VITEK 2 automated identification (ID) and antibiotic susceptibility test- ALERT microbial detection system infections include Enterobacteriaceae (bioMérieux). Samples were inoculated such as Escherichia coli, Klebsiella pneu- ing (AST) systems, the MicroScan ID and AST panels, fluorescencein situ into BacT/ALERT standard aerobic moniae and Pseudomonas aeruginosa and standard anaerobic blood culture (6). Among Gram-positive bacterial hybridization (FISH) and polymerase chain reaction (PCR) analyses (8–12). bottles, which were transferred to the infections, Staphylococcus aureus and co- BACTEC™ 9240 blood culture system, The VITEK system used in the pre- agulase-negative staphylococci are the software version V4.70A (Becton Dick- sent study was developed by bioMérieux­ predominant causative agents, but inson) for monitoring bacterial growth. as an automated system for identifica- other bacteria, such as enterococci and Positive blood cultures containing tion and antimicrobial susceptibility streptococci can also be associated (7). Gram-negative rods and Gram-positive testing and was later improved into the Minor bloodstream infections can be cocci that appeared monomicrobial VITEK 2 system. The improved version managed by the immune system, but in the Gram stain were included in the automates all mandatory steps for iden- severe infections need to be treated study. In total, 233 positive aerobic tification and antimicrobial susceptibil- with antibiotics. The increasing rate of blood cultures were analysed, including ity testing after a standardized inoculum multidrug-resistant bacteria associated 166 cultures with Gram-negative bacilli with bacteraemia, however, is raising has been loaded into the system (13). and 74 with Gram-positive cocci. serious concerns (6). The samples are read every 15 min. by a In order to determine the best kinetic analysis of fluorescence, turbidity Direct identification of treatment for a patient, it is important and colorimetric signals. The results are bacteria using the VITEK 2 ID to carry out proper identification and available within 3 h for identification and system susceptibility testing of the causative 2.5–18 h for susceptibility testing. The bacteria were directly identified agents. However, the rapidity with Various studies have evaluated the using samples from the blood culture which the identification and suscep- performance of the VITEK 2 system bottles that were incubated for 4–24 tibility testing are done is critical for a for identification of Gram-negative h at 35 °C. From each bottle, 3 mL or positive outcome for the patient and and -positive bacteria associated with 9 mL fluid (for Gram-positive cocci) hence for decreasing the mortality and bacteraemia (13,14), but the results were sampled and first centrifuged at morbidity rate associated with such vary across studies. This variability does 150× g for 10 min. in order to isolate infections. Various methods have been not allow clear and definite conclusions the blood cells (in the pellet). Then

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the bacteria cells were harvested by gentamicin, oxacillin, penicillin, trimeth- ATCC 29213 were used as reference centrifuging (at 1000× g for 10 min.) a oprim-sulfamethoxazole, teicoplanin strains for quality controls. mixture of 2 mL supernatant with 1 mL and vancomycin. Analysis of the identification and sus- of 0.45% saline to eliminate residual red ceptibility testing of bacteria blood cells by lysis. A bacterial suspen- Identification & susceptibility testing of bacteria by the To screen the accuracy of the direct sion was prepared by mixing the pellet standard method identification and susceptibility test- with 0.45% saline to obtain a concentra- ing of bacteria in the blood samples, tion of 0.5–0.63 McFarland units using To determine the accuracy of the direct the VITEK 2 standard and VITEK 2 the VITEK DensiCHEK™ colorimeter identification and susceptibility testing direct methods were compared. For (bioMérieux). When no bacterial pellet of bacteria in the blood samples, the the bacteria identification, the results was observed after the second centrifu- microorganisms were also screened by of the VITEK 2 standard method were gation for Gram-positive bacteria, 1.5 a standard method. For this purpose, used as the reference, except in a few mL of 0.45% saline and 3 mL of brain- blood and chocolate agar plates were cases where the API system results were heart infusion were added and the tube inoculated with about 0.1 mL of cul- necessary to provide a definitive identifi- incubated under shaking at 37 °C for 2 ture liquid from a blood culture bottle, cation. Only bacteria that were correctly h to induce a better growth. followed by an overnight incubation at 35 °C in 5% carbon dioxide. The identified by the standard method were The suspensions (2 mL) were auto- bacterial suspension for each isolate included in the comparison. The results matically loaded into the VITEK 2 ID was then prepared and the turbidity from the direct identification method system (bioMérieux), using the GNB adjusted to match that of a McFarland were reported as: correctly identified; and GPC cards for identification of 0.5–0.63 standard in 0.45% sterile misidentified; or not identified. In the Gram-negative rods and Gram-positive sodium chloride solution. The suspen- VITEK 2 ID system, K. pneumoniae cocci respectively and the version 2.01 sions (2 mL) were loaded into the ap- subsp. pneumoniae (planticola/terrigena) release software. The cards were read by propriate VITEK 2 ID and AST cards and K. pneumoniae subsp. ozaenae were kinetic fluorescence measurement and as described above. considered identical and reported as K. the results reported within 3 h. pneumoniae. For comparison with the standard Direct testing of antimicrobial method using the VITEK 2 ID cards For the susceptibility testing, the susceptibility of bacteria using and for bacteria that were not identi- results of the direct method were classi- the VITEK 2 AST system fied by that method, analytical profile fied into 4 groups: category agreement For the susceptibility testing, only index (API) identification systems (complete agreement between the two bacteria correctly identified with the (bioMérieux) were used. Enterobacte- methods); minor discrepancy (suscep- VITEK 2 ID system were included in riaceae were identified with API 20E, tible or resistant by the direct method the experiments. Then 2 mL samples non-fermenters with API 20NE, Ente- and intermediate by the standard of each suspension were prepared as rococcus spp. and Streptococcus spp. with method or vice versa); major discrep- described above and were automati- API Strep, Micrococcus spp. and Staphy- ancy (resistant by the direct method but cally loaded into the VITEK 2 AST lococcus spp. with API Staph. sensitive by the standard method); and very major discrepancy (sensitive by system (bioMérieux) using the GN04 For the susceptibility testing, the the direct method but resistant by the and P526 cards for susceptibility testing bacteria were additionally tested against standard method). of Gram-negative rods and for Gram- the antimicrobials mentioned above positive cocci respectively and the 2.01 using the broth microdilution method, release software. The cards were read by according to guidelines and break- Results kinetic fluorescence measurement and points set by the Clinical and Labora- the results reported within 2.5–16.25 h. tory Standards Institute. The inoculum Identification of Gram- A total of 10 antimicrobials were concentration was 105 colony-forming negative rods & Gram-positive screened for Gram-negative rods: ampi- units/mL and an appropriate broth was cocci by the standard method cillin, aztreonam, cefepime, ceftazidime, used for each type of bacteria. By the standard method, 166 Gram- ceftriaxone, imipenem, ciprofloxacin, negative bacteria were identified and gentamicin, amikacin, and trimetho- Quality control tested (Table 1). These included 113 prim-sulfamethoxazole. For Gram- For all experiments performed with isolates of Enterobacteriaceae and 53 positive cocci, the susceptibility against both VITEK 2 ID and VITEK 2 AST non-fermenting bacteria. Enterobacte- 9 antimicrobials was investigated: cip- cards, E. coli (ATCC) 25922, P. aer- riaceae species included E. coli, Ent. fae- rofloxacin, clindamycin, erythromycin, uginosa ATCC 27853, and Staph. aureus calis, Ent. cloacae, K. pneumonia, K. oxytoca

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Table 1 Identification of Gram-negative bacilli using VITEK® 2 ID-GNB cards inoculated with culture fluids from positive blood culture bottles Isolate Correctly VNGNB Not identified Misidentified tested identified

No. No. % No. % No. % No. % Enterobacteriaceae Escherichia coli 38 38 100.0 0 0.0 0 0.0 0 0.0 Enterobacter faecalis 14 13 92.9 0 0.0 0 0.0 1 7. 7 Enterobacter cloacae 3 3 100.0 0 0.0 0 0.0 0 0.0 Klebsiella pneumoniae 46 44 95.7 0 0.0 0 0.0 2 4.5 Klebsiella oxytoca 1 1 100.0 0 0.0 0 0.0 0 0.0 Salmonella spp. 9 9 100.0 0 0.0 0 0.0 0 0.0 Aeromonas spp. 2 2 100.0 0 0.0 0 0.0 0 0.0 Total 113 110 97.3 0 0.0 0 0.0 3 2.7 Non-fermenters Acinetobacter baumannii 42 40 95.2 2 4.8 0 0.0 0 0.0 Chryseobacterium indologenes 1 1 100.0 0 0.0 0 0.0 0 0.0 Pseudomonas aeruginosa 10 8 80.0 2 20 0 0.0 0 0.0 Total 53 49 92.5 4 7. 5 0 0.0 0 0.0 All types 166 159 95.8 4 2.4 0 0.0 3 1.8

VNGNB = various non-fermenting Gram-negative bacilli.

and isolates of the genus Salmonella Gram-negative bacteria investigated, with the standard method (Table 2), and Aeromonas. The non-fermenters in- 95.8% (159/166) showed concord- the comparative analysis revealed that cluded Acinetobacter baumannii, Chryseo- ant results with the standard method, 89.2% (66/74) of the bacteria were bacterium indologenes and P. aeruginosa. 2.4% (4/166) were classified as vari- correctly identified, 6.8% (5/74) not A total of 74 Gram-positive cocci were ous non-fermenting Gram-negative identified and 4.1% (3/74) misiden- identified and tested (Table 2), includ- bacilli and 1.8% (3/166) were misi- tified. It was noticed that although ing 14 isolates of the genus Enterococcus dentified. For bacteria of the family the majority of isolates were correctly (Ent. faecalis and Ent. faecium), 45 of Enterobacteriaceae, 97.3% (110/113) identified, the percentage success was the genus Staphylococcus (Staph. aureus, were correctly identified and 2.7% 6.6% less than the success rate ob- Staph. epidermidis, Staph. haemolyticus (3/113) were misidentified (1 isolate tained for the Gram-negative bacteria. and coagulase-negative staphylococci of Ent. faecalis and 2 of K. pneumonia). The bacteria that were not identified ), 12 of the genus Streptococcus (Strep. Enterobacter faecalis was misidentified by the direct method included 2 agalactiae, group D streptococci and as Kleibseilla sp. and K. pneumonia as isolates of Staph. aureus and 1 each Strep. pneumoniae) and 3 of the genus Enterococcus spp. Of the non-fermenter for Ent. faecalis, group D streptococci Micrococcus. bacteria 92.5% (49/53) were correctly and Strep. pneumoniae. Only 3 isolates identified and 7.5% were reported as of coagulase-negative staphylococci Direct identification of Gram- various non-fermenting Gram-nega- were misidentified: 1 as Corynebac- negative rods using the VITEK terium spp. and 2 as Micrococcus spp. 2 ID-GNB card tive bacilli (2 isolates of A. baumannii and 2 of P. aeruginosa). With regards to each group of cocci, The Gram-negative bacteria identi- 92.9% of enterococci (13/14) were fied by the standard method were also Direct identification of Gram- successfully identified and 7.1% were investigated by a direct inoculation positive cocci using the VITEK not identified. For theStaphylococcus of culture fluids from positive blood 2 ID-GPC card spp., 88.9% (40/45) were correctly cultures into VITEK 2 ID- GNB cards. The Gram-positive cocci identified by identified, 4.4% (2/45) not identified Comparing with the standard method, the standard method were also investi- and 6.7% misidentified (3/45). For the analysis revealed that most bac- gated by a direct inoculation of culture the Streptococcus spp., 83.3% (10/12) teria were successfully identified. fluids from positive blood cultures into were correctly identified and 16.7% As seen in Table 1, among the 166 VITEK 2 ID-GPC cards. Comparing (2/12) not identified. All 3 isolates

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Table 2 Identification of Gram-positive cocci using VITEK® 2 ID-GPC cards inoculated with culture fluids from positive blood culture bottles Bacteria Isolates Correctly identified Not identified Misidentified tested No. No. % No. % No. % Enterococci Enterococcus faecalis 11 10 90.9 1 9.1 0 0.0 Enterococcus faecium 3 3 100.0 0 0.0 0 0.0 Total 14 13 92.9 1 7. 1 0 0.0 Micrococcus spp. 3 3 100.0 0 0.0 0 0.0 Staphylococci Staphylococcus aureus 31 29 93.5 2 6.5 0 0.0 Staphylococcus epidermidis 2 2 100.0 0 0.0 0 0.0 Staphylococcus haemolyticus 4 4 100.0 0 0.0 0 0.0 Coagulase-negative staphylococci 8 5 62.5 0 0.0 3 37.5 Total 45 40 88.9 2 4.4 3 6.7 Streptococci Streptococcus agalactiae 2 2 100.0 0 0.0 0 0.0 Group D streptococci 4 3 75.0 1 25.0 0 0.0 Streptococcus pneumoniae 6 5 83.3 1 16.7 0 0.0 Total 12 10 83.3 2 16.7 0 0.0 All types 74 66 89.2 5 6.8 3 4.1

belonging to the genus Micrococcus seen for ampicillin, ceftazidime and Regarding individual antimicrobials, were correctly identified. ceftriaxone. the highest rate of discrepancy was seen for clindamycin, with mainly minor Susceptibility testing of Susceptibility testing of and major discrepancies. Very major Gram-negative bacteria to Gram-positive bacteria to antimicrobials using the VITEK antimicrobials using the VITEK discrepancies were only observed for 2 AST-GN04 card 2 AST-P526 card gentamicin, oxacillin and erythromycin. For the susceptibility testing, only cor- Similarly to the susceptibility testing of rectly identified bacteria were consid- the Gram-negative bacteria, only suc- Discussion ered (n = 159). The results obtained by cessfully identified bacteria were con- the standard method were compared sidered (n = 67). The results obtained The present study revealed that the with those obtained with the direct by the standard method were compared accuracy of the VITEK 2 system for method (Table 3). The 159 isolates with those obtained with the direct a direct identification and susceptibil- were evaluated for their susceptibil- method (Table 4). The 66 isolates were ity testing in blood cultures of Gram- ity to 10 antimicrobials, resulting in evaluated for their susceptibility to 9 positive rods and Gram-negative cocci a total of 1590 isolate–antimicrobial antimicrobials resulting in a total of varied according to the type and species compound combinations. The overall 603 isolate–antimicrobial compound level of agreement between the two combinations. The overall level of agree- of bacteria as well as the antimicrobial methods was 92.0%. The highest ment between the two methods was screened. level of agreement was obtained for 91.3%. The highest level of agreement For both types of bacteria, the over- amikacin (98.7%) and the lowest for was obtained for vancomycin (100%) all high level of concordance (95.8% ampicillin, ceftazidime and ceftriaxone and trimethoprim–sulfamethoxazole and 89.2%) between the identification (88.0%). The overall disagreement rate (97.0%) and the lowest rate of agree- results obtained with the standard was 8.6% including 4.9% minor dis- ment was observed for clindamycin and direct methods suggest that the crepancies, 2.9% major discrepancies (82.0%). The overall disagreement VITEK 2 ID system is a suitable tool and 0.8% very major discrepancies. rate was 8.6%, including 4.8% minor for a direct and rapid identification of Regarding individual antimicrobials, discrepancies, 2.8% major discrepan- species of bacteria contained in blood the highest rate of discrepancy was cies and 1.0% very major discrepancies. cultures. Similar results were obtained

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Table 3 Agreement in antimicrobial susceptibility testing between direct and standard methods for Gram-negative bacilli using VITEK® 2 AST-GN04 cards Variable Category Minor discrepancy Major discrepancy Very major agreement discrepancy No. % No. % No. % No. % Antimicrobials (n = 159 isolates tested) Ampicillin 140 88.0 7 – 7 – 5 – Aztreonam 151 95.0 4 – 4 – 0 – Ceftazidime 140 88.0 12 – 7 – 0 – Ceftriaxone 140 88.0 10 – 5 – 4 – Cefepime 148 93.0 3 – 5 – 3 – Imipenem 150 94.3 7 – 2 – 0 – Ciprofloxacin 143 89.9 13 – 3 – 0 – Gentamicin 151 95.0 6 – 2 – 0 – Amikacin 157 98.7 2 – 0 – 0 – Trimethoprim–sulfamethoxazole 143 89.9 8 – 8 – 0 – Total (n =1590 isolate–antimicrobial 1463 92.0 72 4.9 43 2.9 12 0.8 combinations)

by various previous studies in which comparison with the corresponding between the standard method and a high level of correlation between cards tested by a standard method direct methods for the susceptibility the two methods were observed. (19). Chen et al. recommended the testing of the studied bacteria to an- For Gram-negative rods, Chen et al. use of the VITEK 2 system for Gram- timicrobials. The agreement of up to reported a correlation rate of 89.7% negative rods but not for Gram-posi- 92.0% and 91.3% for Gram-negative (8), Ling et al. reported a correlation tive cocci (8). De Cueto et al. justified rods and Gram-positive cocci respec- rate of 95% and (15) Bruins et al. a the difference between their results tively correlate with previous findings correlation of 93.0%, (16). For Gram- and those of studies with a high cor- in which 80–100% category agree- positive cocci, the present study results relation rate by a difference in blood ment was observed (8,15–17,20). correlate with those of Ligozzi et al. cultures, conventional identification The high rate of concordance ob- whereby more than 90% of Gram- systems and techniques for inoculum served in the current study and some positive cocci were identified within 3 preparation from the blood culture of the earlier reports can be partly at- h by the VITEK 2 ID system with up bottles 19( ). Some procedures for tributed to the fact that only correctly to 99% identification correlation rate inoculum preparation may not be ap- identified bacteria were included in for Staph. aureus (17). Lupetti et al. propriate for a complete removal of the susceptibility testing. In fact, in (14) and Funke and Funke-Kissling substances which may interfere with studies which included unidentified (18) also reported a rate of 89–97% the fluorescent biochemical reactions and misidentified microorganisms, correctly identified Gram-positive occurring in the VITEK 2 cards. a much lower category agreement cocci. However, a study by de Cueto et for Gram-negative rods (50%) and In the present study, the level of al. reported a much lower correlation Gram-positive cocci (38%) was rate of 62% for Gram-negative bacilli disagreement between the two iden- observed (19). The present study and a complete disagreement (0%) for tification methods was higher for results demonstrated that the level the Gram-positive cocci (14). Chen Gram-positive bacteria than Gram- of category agreement and errors for et al. also reported a correlation rate negative rods. This phenomenon has the susceptibility testing were almost of 33% for Gram-positive cocci with been previously observed (8,19) and similar for both Gram-negative rods 9 and 33 isolates out of 63 not identi- was attributed to the difficulty to ob- and Gram-positive cocci, thereby con- fied and misidentified respectively8 ( ). tain sufficient numbers of bacteria to tradicting the findings of Chen et al., De Cueto et al. concluded that the reach the required VITEK 2 McFar- who found that the rate of errors was VITEK 2 ID cards inoculated directly land concentration. much higher for Gram-positive cocci with positive Bactec 9240 bottle fluids Similar to the bacteria identifica- than Gram-negative bacilli (8). The do not provide an acceptable identi- tion results, an overall high level of investigation reported here suggests fication for both types of bacteria in category agreement was observed that the VITEK 2 system provides

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Table 4 Agreement in antimicrobial susceptibility testing between direct and standard methods for Gram-positive cocci using VITEK® 2 AST-P526 cards Variable Category Minor discrepancy Major discrepancy Very major agreement discrepancy No. % No. % No. % No. % Antimicrobials (n = 67 isolates tested) Clindamycin 55 82.0 8 – 4 – 0 – Ciprofloxacin 57 85.0 7 – 3 – 0 – Erythromycin 60 89.5 5 – 1 – 1 – Gentamicin 60 89.6 4 – 0 – 3 – Oxacillin 61 91.0 0 – 4 – 2 – Penicillin 63 94.0 0 – 4 – 0 – Trimethoprim–sulfamethoxazole 65 97.0 1 – 1 – 0 – Teicoplanin 63 94.0 4 – 0 – 0 – Vancomycin 67 100.0 0 – 0 – 0 – Total (n = 603 isolate–antimicrobial 551 91.3 29 4.8 17 2.8 6 1.0 combinations)

accurate susceptibility testing results, and incorrect characterization of pol- methods, which have been reported since the overall rates of agreement ymicrobial cultures as monomicrobial not to be fully reliable for an accurate with the standard method were above (8,19). The Gram staining commonly identification of bacteria 22( ). 90% and the rates of discrepancies used to separate polymicrobial and In other studies the identification below 3% for major and 1.5% for very monomicrobial cultures may some- of bacteria by the use of molecular bi- major discrepancies, as stated in the times lead to errors. In the present ology methods such as FISH and PCR guidelines for the assessment of the study, only monomicrobial cultures has been shown to be more reliable for performance of antimicrobial suscep- were investigated and standardized the identification of microorganisms tibility tests (21). With regards to the inoculum was used. It has been also in general and also for those respon- level of agreement for individual anti- reported that the slower metabolism sible for blood infections (9,23,24). microbials, a variation of agreement/ of some bacteria such as non-enteric Nevertheless the present study results, discrepancy is observed from one and non-fermenting bacteria as well along with other studies (10,25), in- study to another and this may be re- as coagulase-negative staphylococci dicate that the VITEK 2 system has lated to species or subspecies or strain can cause more errors in their iden- an overall reliable performance and specificity. Nonetheless, occurrence tification/susceptibility testing using it is safe enough to allow immediate of very major errors seem to be recur- the VITEK 2 system (13,15,17). This reporting. It is expected that a ma- rent when testing the susceptibility to is due to the fact that the slow me- jor reduction in the time required to some antimicrobials such as ampicillin tabolism causes weaker fluorescent determine the correct treatment for for Gram-negative bacilli (8,19). On biochemical reactions in the VITEK 2 patients’ infections will lead to reduc- the other hand, the absence or very card reaction wells (15). tions in patient mortality and in overall low rate of errors for the susceptibility The results of the study reported hospital costs (10). testing of Gram-positive cocci toward here suggest that the VITEK 2 system vancomycin is common (8,14,19). is a suitable tool for a rapid and direct Using the VITEK 2 system some identification and susceptibility test- Acknowledgements bacteria in our study were not identi- ing of Gram-negative rods and Gram- fied or were misidentified and various positive cocci from blood samples. Funding: We would like to thank levels of disagreement in the suscepti- However, as recommended by Ling et Philadelphia University, Amman, and bility testing were found. According to al. and Funke et al. (13,15), the system Princess Iman Research and Labora- De Cueto et al. and Chen et al. these should be improved for slower meta- tory Sciences Centre, Royal Medical errors can be related to factors such as bolic bacteria. The VITEK 2 system Services, Amman, for their support and the use of non-standardized inoculum error rates are usually based on a com- cooperation in conducting this research. size or low concentrations of inoculum parison with conventional phenotypic Competing interests: None declared.

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References

1. Reimer LG, Wilson ML, Weinstein MP. Update on detec- 14. Lupetti A, Barnini S, Castagna B, Capria AL, Nibbering PH. tion of bacteremia and fungemia. Clin Microbiol Rev. 1997 Rapid identification and antimicrobial susceptibility profil- Jul;10(3):444–65. PMID:9227861 ing of Gram-positive cocci in blood cultures with the Vitek 2 2. Orsini J, Mainardi C, Muzylo E, Karki N, Cohen N, Sakou- system. Eur J Clin Microbiol Infect Dis. 2010 Jan;29(1):89–95. las G. Microbiological profile of organisms causing blood- PMID:19902279 stream infection in critically ill patients. J Clin Med Res. 2012 15. Ling TK, Liu ZK, Cheng AF. Evaluation of the VITEK 2 system for Dec;4(6):371–7. PMID:23226169 rapid direct identification and susceptibility testing of Gram- 3. Kinane DF, Riggio MP, Walker KF, MacKenzie D, Shearer B. negative bacilli from positive blood cultures. J Clin Microbiol. Bacteraemia following periodontal procedures. J Clin Peri- 2003 Oct;41(10):4705–7. PMID:14532207 odontol. 2005 Jul;32(7):708–13. PMID:15966875 16. Bruins MJ, Bloembergen P, Ruijs GJ, Wolfhagen MJ. Identifi- 4. Peleg AY, Hooper DC, Hooper DC. Hospital-acquired infec- cation and susceptibility testing of Enterobacteriaceae and tions due to gram-negative bacteria. N Engl J Med. 2010 May Pseudomonas aeruginosa by direct inoculation from positive 13;362(19):1804–13. PMID:20463340 BACTEC blood culture bottles into Vitek 2. J Clin Microbiol. 2004 Jan;42(1):7–11. PMID:14715724 5. Maschmeyer G, Noskin GA, Ribaud P, Sepkowitz KA. Chang- ing patterns of infections and antimicrobial susceptibilities. 17. Ligozzi M, Bernini C, Bonora MG, De Fatima M, Zuliani J, Oncology (Williston Park). 2000 Aug;14(8) Suppl 6:9–16. Fontana R. Evaluation of the VITEK 2 system for identification PMID:10989819 and antimicrobial susceptibility testing of medically relevant gram-positive cocci. J Clin Microbiol. 2002 May;40(5):1681–6. 6. Kang CI, Kim SH, Park WB, Lee KD, Kim HB, Kim EC, et al. Blood- PMID:11980942 stream infections caused by antibiotic-resistant gram-negative bacilli: risk factors for mortality and impact of inappropriate 18. Funke G, Funke-Kissling P. Performance of the new VITEK 2 initial antimicrobial therapy on outcome. Antimicrob Agents GP card for identification of medically relevant Gram-positive Chemother. 2005 Feb;49(2):760–6. PMID:15673761 cocci in a routine clinical laboratory. J Clin Microbiol. 2005 Jan;43(1):84–8. PMID:15634954 7. Fitzgibbons LN, Puls DL, Mackay K, Forrest GN. Management of gram-positive coccal bacteremia and hemodialysis. Am J 19. de Cueto M, Ceballos E, Martinez-Martinez L, Perea EJ, Pascual Kidney Dis. 2011 Apr;57(4):624–40. PMID:21333430 A. Use of positive blood cultures for direct identification and susceptibility testing with the vitek 2 system. J Clin Microbiol. 8. Chen JR, Lee SY, Yang BH, Lu JJ. Rapid identification and sus- 2004 Aug;42(8):3734–8. PMID:15297523 ceptibility testing using the VITEK 2 system using culture fluids from positive BacT/ALERT blood cultures. J Microbiol Immu- 20. Hansen DS, Jensen AG, Nørskov-Lauritsen N, Skov R, Bruun B. nol Infect. 2008 Jun;41(3):259–64. PMID:18629422 Direct identification and susceptibility testing of enteric bacilli from positive blood cultures using VITEK (GNI+/GNS-GA). Clin 9. Wellinghausen N, Bartel M, Essig A, Poppert S. Rapid iden- tification of clinically relevant Enterococcus species by Microbiol Infect. 2002 Jan;8(1):38–44. PMID:11906499 fluorescence in situ hybridization. J Clin Microbiol. 2007 21. Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH. Oct;45(10):3424–6. PMID:17670922 Manual of clinical microbiology. Washington (DC): American 10. Quesada MD, Giménez M, Molinos S, Fernández G, Sánchez Society for Microbiology Press; 1999. MD, Rivelo R, et al. Performance of VITEK-2 Compact and 22. Towner KJ, Cockayne A. Molecular methods for microbial overnight MicroScan panels for direct identification and sus- identification and typing. London: Chapman and Hall; 1999. ceptibility testing of Gram-negative bacilli from positive FAN 23. Bosshard PP, Zbinden R, Abels S, Böddinghaus B, Altwegg M, BacT/ALERT blood culture bottles. Clin Microbiol Infect. 2010 Böttger EC. 16S rRNA gene sequencing versus the API 20 NE Feb;16(2):137–40. PMID:19778301 system and the VITEK 2 ID-GNB card for identification of non- 11. Tsalik EL, Jones D, Nicholson B, Waring L, Liesenfeld O, Park fermenting Gram-negative bacteria in the clinical laboratory. J LP, et al. Multiplex PCR to diagnose bloodstream infections Clin Microbiol. 2006 Apr;44(4):1359–66. PMID:16597863 in patients admitted from the emergency department with 24. Kaleta EJ, Clark AE, Johnson DR, Gamage DC, Wysocki VH, sepsis. J Clin Microbiol. 2010 Jan;48(1):26–33. PMID:19846634 Cherkaoui A, et al. Use of PCR coupled with electrospray ioni- 12. Jordana-Lluch E, Carolan HE, Giménez M, Sampath R, Ecker zation mass spectrometry for rapid identification of bacterial DJ, Quesada MD, et al. Rapid diagnosis of bloodstream infec- and yeast bloodstream pathogens from blood culture bottles. tions with PCR followed by mass spectrometry. PLoS One. J Clin Microbiol. 2011 Jan;49(1):345–53. PMID:21048006 2013;8(4):e62108. PMID:23626775 25. Spanu T, Sanguinetti M, Ciccaglione D, D’Inzeo T, Romano 13. Funke G, Monnet D, deBernardis C, von Graevenitz A, Freney L, Leone F, et al. Use of the VITEK 2 system for rapid iden- J. Evaluation of the VITEK 2 system for rapid identification of tification of clinical isolates of Staphylococci from blood- medically relevant gram-negative rods. J Clin Microbiol. 1998 stream infections. J Clin Microbiol. 2003 Sep;41(9):4259–63. Jul;36(7):1948–52. PMID:9650942 PMID:12958254

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Review Routine immunization services in Pakistan: seeing beyond the numbers S. Husain 1 and S.B. Omer 2

خدمات التحصني الروتيني يف باكستان: رؤية ملا وراء األرقام سارا حسني، سعد بن عمر اخلالصــة:ال تــزال األمــراض التــي يمكــن الوقايــة منهــا باللقاحــات ًســببا ً رئيســياللمراضــة والوفيــات لــدى األطفــال الذيــن تقــل أعمرهــم عن 5 ســنوات يف باكســتان، وال يــزال هــذا البلــد أحــد آخــر مســتودعات شــلل األطفــال، ممــا يشــكل ًهتديــدا بانتشــار الفــريوس يف املنطقــة والعــامل. وهــذا االســتعراض املنظــم يبــ ِّني التحديــات التــي تواجــه حتقيــق األهــداف املرجــوة مــن التحصــني، وحيــدد ًأطــرا للسياســات والتدخــات الربناجميــة والبحــوث املســتقبلية. إن برنامــج التحصــني َّاملوســع الــذي ُوضــع ًمؤخــرا - والــذي ينــوء بعــبء حمدوديــة الطلــب وعــدم كفــاءة خدمــات التحصــني - يواجــه العديــد مــن العقبــات التــي حتــول دون زيــادة أحجــام التحصــ ،ني وحتســني جــودة اخلدمــات، والتحصــني يف الوقــت املناســب. فربنامــج التحصــني املوســع يتطلــب تدخــات منســقة - متعــددة اجلوانــب، متعــددة املســتويات - لتحســني أداء الربنامــج وتعزيــز اإلقبــال عــى التحصــني عــى مســتوى املجتمــع.باإلضافــة إىل ذلــك، فــإن عــدم وجــود حتقيــق علمــي دقيــق بشــأن خدمــات التحصــني حيــد مــن إدخــال تدخــات اســتجابة متطــورة. إن هــذه الورقــة توضــح املــآزق البنيويــة، وتقــرح احللــول املمكنــة، وتشــري إىل مزيــد مــن خيــوط التحقيــق، لفهــم أســباب انخفــاض معــدالت التحصــني يف باكســتان وتقليصهــا.

ABSTRACT Vaccine-preventable diseases continue to be a major cause of morbidity and mortality among children under 5 years of age in Pakistan, and the country remains one of the last reservoirs of polio, posing a threat of viral spread within the region and globally. This structured review describes challenges in the achievement of vaccination targets and identifies arenas for policy and programmatic interventions and future research. Burdened with limited demand and inefficient vaccination services, the recently devolved Expanded Programme on Immunization (EPI) faces multiple hurdles in increasing immunization volumes, improving the quality of services and ensuring timely vaccination. The EPI requires multi-pronged, multi-level, coordinated interventions to improve programme functioning and to enhance vaccination uptake at community level. Additionally, a lack of rigorous scientific enquiry on vaccination services limits the introduction of well-developed, responsive interventions. The paper describes systemic bottlenecks, proposes potential solutions and suggests lines of further enquiry to understand and reduce the languishing immunization rates in Pakistan.

Les services de vaccination systématique au Pakistan : voir au-delà des chiffres

RÉSUMÉ Les maladies à prévention vaccinale demeurent l’une des causes principales de morbidité et de mortalité parmi les enfants de moins de 5 ans au Pakistan, et le pays constitue l’un des derniers réservoirs de poliomyélite, représentant ainsi une menace de propagation des virus à l’échelle régionale et mondiale. Cet examen structuré décrit les défis inhérents à la réalisation des objectifs de la couverture vaccinale, et identifie les domaines qui requièrent des interventions politiques et programmatiques ainsi que de plus amples travaux de recherche. Du fait d’une faible demande et de l’inefficacité des services de vaccination, le Programme élargi de vaccination (PEV), récemment décentralisé, est confronté à de multiples obstacles dans sa démarche d’augmentation des vaccinations, d’amélioration de la qualité des services et d’administration de vaccins en temps voulu. Le PEV requiert des interventions coordonnées sur plusieurs fronts et à tous les niveaux pour améliorer son fonctionnement et augmenter l’acceptation des vaccins au niveau communautaire. De plus, un manque d’investigations scientifiques rigoureuses sur les services de vaccination empêche la mise en place d’interventions bien conçues et adaptées. La présente étude recense les obstacles systémiques, propose des solutions potentielles et suggère des axes de recherche à approfondir afin de comprendre les éléments qui entraînent la stagnation des taux de vaccination au Pakistan et d’inverser la tendance.

1Department of Paediatrics and Child Health, Aga Khan University, Karachi, Pakistan (Correspondence to S. Husain: sara.husain @aku. edu). 2Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America. Received: 03/12/15; accepted: 21/12/15

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Introduction “expanded programme on immuniza- immunization in Pakistan followed by tion” and “Pakistan”. The search included an analysis of health system bottlenecks A low–middle income country of South all relevant articles concerning human that affect routine immunization ser- Asia, Pakistan is one of the few countries subjects and published in English lan- vices. in the world with persistent circulation guage from 1995 to 2015. A total of 410 of poliovirus, posing a threat to global articles were identified, of which 271 polio eradication initiatives (1). Home referred to immunization in Pakistan Results to one of the largest birth cohorts in in either the title or abstract. Of these, Structure of vaccination articles pertaining to adult vaccinations the developing world (2), Pakistan services in Pakistan continues to struggle to improve rou- (3 articles), specific vaccine-preventable tine immunization services among its illnesses (162 articles), vaccine effective- Established as a vertical programme in under-2-year-old population of more ness studies (8 articles), molecular vac- 1978, the EPI in Pakistan began with than 10 million (3,4). The sheer size cine development studies (24 articles), smallpox eradication and was rapidly of the target population presents an duplicate studies (30 articles) and those followed by the introduction of 5 anti- opportunity to intervene and achieve not available online (2 articles) were gens within the national immunization significant reductions in infant and child excluded. The final analysis included 38 schedule (5,6; deputy manager EPI mortality at the local and regional level. articles addressing childhood routine programme, Sindh province, unpub- lished presentation, 2014). Currently, Although a significant body of work immunization services in Pakistan, the the programme offers a series of 9 anti- exists on childhood immunization in majority of which (35 articles) were gens from birth to 2 years of age (Table Pakistan, most studies have looked at descriptive studies conducted in vari- 1). Overwhelmingly provided by the individual vaccines (polio, tetanus, ro- ous settings in Pakistan. Only 3 articles public sector (7), vaccination services in tavirus, etc.) and we are not aware of a reported the results of randomized con- Pakistan are delivered by several cadres comprehensive review of the health sys- trolled trials conducted in peri-urban of health workers (8). tem determinants of low immunization and rural settings. coverage. Significantly, no publication Grey literature on the subject was Vaccinators form the primary addresses the programmatic changes identified by reviewing the references in workforce for routine immunization in that have been made subsequent to the identified scientific literature and by pre-determined catchment areas (with recently enacted devolution of the contacting academic and public health reference to health facilities) and out-of- public health system. With mounting institutes involved in EPI and systems catchment areas through facility-based international and local efforts targeting research in Pakistan. The work iden- and outreach services. Each vaccinator vaccination services in Pakistan, and in tified included assessments done by is monitored and supervised by the tehsil order to identify bottlenecks affecting the United Nations Children’s Fund (sub-district) and district level supervi- programme function, we present a re- and the GAVI Alliance, serial Pakistan sors along with district and provincial view paper discussing the current status Demographic and Health Surveys, the EPI programme managers through of childhood vaccination in Pakistan Pakistan Social and Living Standards field and facility-based visits. Additional and the renewed role of the expanded Measurement Survey, and provin- cadres providing vaccination services programme on immunization (EPI). cial and national country multi-year during special immunization initiatives We expect this paper will fill the existing plans for the EPI. The literature syn- include community-based lady health knowledge gap and provide updated in- thesized below begins with a descrip- workers and facility-based staff includ- formation to national and international tion of the current system and state of ing lady health visitors, dispensers and programme managers, bilateral agencies and researchers interested in immuni- zation-related investments in Pakistan. Table 1 Schedule of the expanded programme on immunization in Pakistan Age of child Immunizations Birth OPV 0, BCG Methods 6 weeks OPV I, Penta I, PCV I 10 weeks OPV II, Penta II, PCV II A literature search for published articles, 14 weeks OPV III, Penta III, PCV III reports and reviews was conducted with 9 months Measles I the PubMed search engine, using the 15 months Measles II

search terms “childhood immuniza- OPV = oral polio vaccine; BCG = bacille Calmette–Guérin; Penta = pentavalent vaccine (diphtheria, pertussis, tion”, “routine vaccination”, “vaccines”, tetanus, hepatitis B, Haemophilus influenza B); PCV = pneumococcal-10 vaccine.

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medical technicians. Data on daily 77% (10–17). Significant interprovin- environment, programme governance service provision, stock utilization and cial and sub-regional variability in vac- and capacity, as discussed below. cold-chain functioning are maintained cine coverage exists (18–22). Punjab, Policy environment through numerous facility-based reg- the most densely populated province, isters and are collated at the end of currently outperforms other provinces, Since 1988, Pakistan and donor the month for submission to higher while coverage has declined over time agencies have invested considerable administrative levels for future service in Sindh and Baluchistan provinces resources into polio eradication, includ- planning and performance assessment. (Figure 1). ing national and sub-national immu- nization days. The emphasis on polio Monthly meetings among vaccination Antigen-specific coverage, although elimination has split immunization staff provide the forum for service and higher than rates of completed vaccina- activities into routine immunization logistics planning and performance tion, shows attrition over serial doses, and polio elimination initiatives, often review. indicating a decline in follow-up vac- perceived as competing activities (26; cination, a pattern unchanged over Status of routine EPI programme manager, Sindh prov- several years ( , , – ). Polio immu- immunization in Pakistan 3 4 23 25 ince, unpublished interview, 2014). One of the foremost programmes nization, however, remains consistently Intense utilization of the public health established in (9), the Pa- high for subsequent doses (Figure 2) machinery and a concentration of re- kistan EPI has shown less than optimal (20). Gains in vaccination coverage sources on polio-focused activities is performance over successive years of over time are concentrated in urban set- widely cited for shifting the focus away the programme, with an estimated 54% tings, resulting in widening urban–rural from routine immunization and causing of children under 2 years completely disparities in vaccination coverage over “polio fatigue” among staff, managers immunized—a rate well below recom- the last 2 decades (Figure 3) (11,22). and the community (19,26,27). There mended levels for universal vaccination Stagnating rates of immunization is, however, little empirical evidence that (3). There is, however, considerable var- result from gaps in vaccine delivery this has negatively impacted routine iation in the reported rates of completed (supply) on the one hand and low up- immunization activities (28). vaccinations in under-2-year-olds, with take by the population (demand) on Public–private partnerships for ser- the Pakistan Social and Living Stand- the other hand. Bottlenecks limiting vice provision have gained considerable ards Measurement Survey estimating efficient and equitable delivery of vac- mileage in Pakistan. With nearly all prov- rates of 81% and smaller observational cination services result from a complex inces practising some form of public– studies estimating rates from 45% to interplay of factors including the policy private partnership at basic health units,

70 66

60 54 53 53

50 47 47

39 37 38 40 35 35 1991-1990 % 29 2007-2006 30 25 2013-2012 18 20 16

10

0 Pakistan Punjab Sindh KPK Baluchistan

Figure 1 Vaccine coverage (all basic vaccinations) among children aged 12–23 months in Pakistan provinces. Source: Pakistan Demographic and Household Surveys 1990–1991, 2006–2007 and 2013–2014

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service uptake in outsourced facilities 61

60 has increased (29). However, the lim- 1.0 Measles 50 ited scope of contractual obligations and a separation of administrative oversight of vaccinators effectively re- 51 moved them from direct oversight and 57 3.0 supervision by facility-based physicians at outsourced facilities, and vaccination coverage in these areas has remained 57 unchanged (30). 64 2.0

Hep B An exclusive focus on provision of vaccination services through public sector facilities places an immense bur- 62 den on already constrained resources 71 1.0 and excludes the private sector, a major provider of health care in the Pakistani context (9,27). However, involvement 85 of this largely unregulated sector is 83 3.0 challenging, because the partnership 43 raises questions of service quality, effec- tive monitoring and ensuring equity of

89 access to vaccination services (31). As 2013 – 2012 91 2.0 a standalone vertical programme for 61 childhood immunization, the EPI has poor integration at different service Polio

92 delivery points, resulting in significant 93 1.0

2007 – 2006 missed opportunities among women

65 and children seeking medical services for unrelated health issues (17,27; EPI

69 programme manager, Sindh province, 56

0.0 unpublished interview, 2014). 1991 – 1990 12 The last census of Pakistan was conducted in 1998; projections of

65 population demographics, vaccine re- 59

3.0 quirements, procurement and distribu-

43 tion are based on outdated figures and there has been no systematic attempt to rationalize projected requirements by 73 revising population estimates (5,17). 67 2.0 DPT

60 Outdated formulae for estimating population growth and the poor quality of vaccine coverage data seriously limit 79 decision-making at all levels. 75 1.0

64 Programme structure and management

85 Pakistan’s public health system has un- 80

BCG dergone considerable transformation 70 with the local governance ordinance Serial antigen-specific vaccination coverage in Pakistan. Source: Pakistan Demographic and Household Surveys 1990–1991, 2006–2007 and 2013–2014. BCG = Bacille and Household Surveys 1990–1991, Pakistan Demographic Serial antigen-specific Pakistan. Source: vaccination in coverage of 2001 followed by the 18th Amend- 0 10 30 50 70 20 40 90 80 60

100 ment to the Constitution of Pakistan in Antigen coverage (%) coverage Antigen

Figure 2 Figure = diphtheria, DTP Hep B = hepatitis tetanus and pertussis; Calmette–Guérin; B 2011. These changes devolved services

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70 66

60 54 50 48 46 44 40 Urban % 30 30 Rural

20

10

0 1991–1990 2007–2006 2013–2012

Figure 3 Urban–rural disparity in vaccination coverage among children 12–23 months of age in Pakistan. Source: Pakistan Demographic and Household Surveys 1990–1991, 2006–2007 and 2013–2014

and management of government de- programme financing, implementation management information systems and partments to local levels, thus increasing and monitoring. However, common- smart-phone monitoring of vaccinators. the local role in health care provision on interest demands for regulation, In the one-window operation for donor the strategic and operational fronts. national and international coordina- coordination at the federal EPI cell, it is Local governance ordinance es- tion, interprovincial coordination and essential that the provinces provide a tablished the district health system, conformity resulted in the federal EPI significant contribution to account for transferring responsibility of service programme being housed within the inter-provincial variability and enable planning, provision, monitoring and Ministry of Health in the period since improved coordination and consensus evaluation from provincial to district the 18th Amendment, as mentioned building at the national level. levels (32,33). While district coordi- in Table 2 (8). After June 2015, when nation officers established EPI targets, most provincial mid-term plans will Programme governance and capacity human resource and bridge financing conclude, each province will be respon- was under provincial purview, causing sible for procurement and distribution Before the 18th Amendment, provincial conflicts in programme prioritization of vaccines along with guidance and su- EPI offices acted on policies and targets and financing 34( ). Reduced federal pervision of districts. To date, however, established by the federal EPI office, and provincial oversight and an absence there has been little progress on devel- distributed vaccine stocks and supplies of district-based cadres for manage- opment of EPI policies and financing to districts, collated district level data, ment and surveillance of EPI activities lines for the programme at provincial monitored service provision and trained resulted in poor coordination of ac- level (30,38–40). staff. Limited involvement in policy de- tivities, hindered the establishment of Donor and partner agencies play velopment, donor engagement, partner clear roles and responsibilities within a significant role in all aspects of pro- coordination and vaccine forecasting, district health departments and resulted gramme operations involving routine compounded by a paucity of manpower in a near stagnation of health indicators immunization and polio elimination to manage and coordinate service de- (34,35). Furthermore, a lack of ring- initiatives, by engaging all tiers of the livery, severely limited the provincial fencing of funding for the EPI at district EPI programme, public sector machin- EPI cells from effectively taking on the level made financing subject to district ery and not-for-profit organizations. mantle of control transferred by the initiative and discretion in the face of Inputs include policy development, 18th Amendment. Furthermore, a lack competing interests (5,26,36,37). programme planning, vaccine and of provincial engagement in coopera- With the 18th Amendment of the cold-chain procurement, deployment tive development of micro-plans with Constitution, the legislative and ex- and training of human resources, de- districts, poor defaulter tracing (identifi- ecutive functions of health and vertical mand generation through civil soci- cation of children who miss a scheduled programmes were completely devolved ety organization, enhanced monitoring vaccine dose by more than 1 month) to the provinces, including developing and improved reporting of services and deficient service monitoring have and implementing provincial policies, through computerized vaccine logistics resulted in weak capacity-building and

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Table 2 Role of the federal expanded programme on immunization (EPI) in Pakistan (after the 18th Amendment of the Constitution of Pakistan). Source: national comprehensive multi-year strategic plan. Source: (8) Programme component Actions Programme management • Development and implementation of national EPI policy • Interprovincial coordination Service delivery • Development of national standards for service delivery and safe vaccination policies Human resource • Establishing accreditation rules and standards Cost and financing • Co-financing commitments (until June 2015) • Mobilization and coordination of donor financing Vaccine, cold-chain and logistics • Procurement of vaccines and injection supplies • Procurement of cold-chain Surveillance and reporting • Consolidation of provincial reports and generation of national reports • Coordination, information collection and sharing at national and international forums Demand generation • Development of national communication strategies and guidelines

restricted collaborative learning at the about vaccines and immunization surroundings) do not offer immuni- provincial and district levels (35,41). services among vaccinators and allied zation services at existing facilities A lack of succession planning, and staff 41( ; EPI programme manager, (5,8,30,38–40). Most vaccination frequent transfers within manage- Sindh province, unpublished interview, points have visual aids, e.g. posters and ment tiers, result in loss of institutional 2014). Despite the existence of waste banners providing information about memory and limit knowledge transfer. management policies in all provinces vaccines to visiting parents. Owing to With no systematic, formal training of Pakistan (30,38–40), safe disposal the limited financial outlay for commu- programmes for management cadres, of used syringes is not stringently prac- nication and advocacy, however, there learning is mostly self-directed and on- tised, highlighting a need for continued are no take-home EPI promotional the-job and managers often lack the rel- education, training and monitoring of materials (8,17,38). Parents are only evant technical knowledge for directing staff on injection hazards and safe dis- provided with vaccination cards which efficient programme operations9 ( ,26). posal of vaccine-related consumables. carry information on administered vac- Unclear roles and responsibilities, poor Vaccinators form the core work- cines and immunization dates. Service programme governance, lack of stew- force for outreach immunization providers often fail to emphasize the ardship at decision-making levels and services. However, significant political importance of these cards to parents, political interference have caused ram- patronage, poor human resource man- resulting in low rates of card retention pant inefficiencies and have hindered agement and limited local ownership and poor knowledge of the purpose EPI performance at nearly all opera- have resulted in workforce maldistri- of cards (21,26,44). When health care tional levels (27,42,43; EPI programme bution and frequent absenteeism. providers inform parents about the due manager, Sindh province, unpublished Poor outreach performance is often dose they often fail to counsel them on interview, 2014). attributed to lack of transport funds; in the importance of completing vaccina- 2012 an estimated 3–5% of programme tions as per the schedule and on dealing Quality of vaccination services expenditure was on transportation, with vaccine side-effects. Pre-induction training of vaccinators including programme operations, logis- Shortages of vaccines, consumables includes EPI schedules, cold-chain tics, monitoring and service provision and recording tools, including EPI cards maintenance and safe injection prac- (18,26,27,30,38–40,43). Vaccinators and registers, also hampers provision tices. Refresher training is conducted often do not develop or update monthly of vaccination services; in 2012 close when a new vaccine is introduced (EPI micro-plans and defaulter lists for ser- to 17% of basic health units and 7% programme manager, Sindh province, vice provision in catchment areas, ac- of rural health centres had fewer than unpublished interview, 2014); there are, counting for a loss to follow-up among 25% of vaccine antigens (45). Bacille however, no opportunities for regular local populations (26,30,38–40,43). Calmette–Guérin and measles vaccine refresher training. Importantly, training Although static vaccination centres vials are opened on designated days on counselling skills, adverse event re- are housed in health facilities, close to reduce wastage, information which porting, defaulter tracing and integrated to 13% of union councils in Pakistan remains poorly communicated to the service provision are not conducted, (the lowest level of government, com- community. Vaccine shortages and resulting in low levels of knowledge prising a village or urban area and its designated days for special vaccinations

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send a negative message to care-seekers districts reporting vaccine coverage ex- Limited geographical access and in- on the future availability of vaccination ceeding 100% (17,18) convenient opening times at EPI centres services and hence deter people from Low vaccine demand also accounts limit patients’ physical access to vaccina- seeking these services. for declining rates of completed vac- tion services (21,25,26). Most public Inefficiencies of cold storage in- cination among children. Vaccine facilities in Pakistan function between clude absent or non-functional cold- demand is correlated with parental 09.00 and 14.00 hours, thus limiting ac- chain equipment, persistent electrical knowledge of vaccine importance, pa- cess to services to a few hours in the day. outages and improper stocking that rental education and socioeconomic Women attending antenatal services, re- potentially limits antigen efficacy. The status (43,47,48). Published data indi- ceiving prenatal tetanus vaccinations or absence of a cold-chain replacement cate that higher maternal education is delivering at a health facility were more plan and a lack of routine examination positively associated with vaccine up- likely to have their children vaccinated of existing units and record-keeping take (4,10,14,22). Despite rising trends (4,10,13,48), indicating that positive on equipment distribution hampers in vaccination uptake over time, the health-seeking behaviours are associ- timely identification and replacement rate of vaccine uptake is slower among ated with improved uptake of services of ailing units (30,40). Additionally, a parents of lower education levels, thus over time and between generations. lack of funds and a paucity of biomedi- highlighting the need to develop ad- Cultural resistance to vaccination cal equipment expertise at district vocacy and communication strategies uptake is fuelled by fear of side-effects, level limits proper maintenance and specifically designed to address caregiv- prior experiences of vaccine side-effects repair of existing cold-chain equipment ers with little educational attainment and local myths of “vaccine-induced in- (26,41,43,46). (Figure 4) (14,21,49–51). fertility” among children. These themes Records of routine immunization It has been widely established that are also packaged in religious messages services provided at public health facili- “belief in the goodness of vaccination” and are propagated by religious leaders, ties are maintained through 11 different is considerably more important for mo- who are often local opinion-makers. paper-based tools used for recording tivating caregivers than scientific knowl- Increasing resistance to vaccination details of daily and monthly EPI ser- edge about vaccines (14,22,48,52–54). uptake particularly for polio vaccina- vices. Often these registers are poorly Mothers unaware of vaccine side-effects tion has been reported in pockets of the maintained and there is no effort to con- were more likely to have their children country, coupled with rising violence firm reported information from nearby vaccinated (22) and, paradoxically, fear targeting polio campaign workers in catchment populations, thus causing of common side-effects was linked to different cities of Pakistan 55( ). reporting errors (5,17,26). Detailed vaccine refusal (14,22), indicating the A summary of the barriers limiting analysis of coverage reports submitted importance of proper counselling of achievement of universal vaccination at sub-district and district level offices caregivers before and after vaccinating in Pakistan and potential avenues for is not routinely conducted, with few a child. action are shown in Table 3.

90 76 80 74 76 69 70 71 70 62 57 60 54 52 50 40 % 39 38 40 31 30

20

10

0 No education Primary Middle Secondary Higher

1991 1990 2007 2006 2013 2012

Figure 4 Effect of caregiver education level on immunization uptake in Pakistan. Source: Pakistan Demographic and Household Surveys 1990–1991, 2006–2007 and 2013–2014

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Table 3 Barriers to achievement of universal vaccination in Pakistan and potential avenues for action Theme Challenges Recommendations

Programme structure • Ambiguous division of roles and • Development of a renewed scope of work and and management responsibilities of EPI activities following provincial procedures for accountability and the 18th Amendment of the Constitution monitoring structures for different tiers and actors of Pakistan involved in EPI service provision • Common pool of funds at district level, • Introduce activity-specific funding for all health making EPI a competitor for funds and programmes including immunization at district making allocations discretionary level to ensure adequate capitalization for target achievement Programme • Limited managerial capacity and trained • Regular, level-specific training for managerial tiers governance and human resources for programme institutionalized by district and provincial health capacity implementation at district and sub- departments district levels • Institutional strengthening with improved • Poorly implemented structures of monitoring and accountability of concerned cadres accountability exacerbated by political of managers and frontline workers patronage and interference Human resources • Lack of rational deployment of trained • GIS mapping of human resources and catchment human resources populations for rational redeployment • Lack of refresher training of • Employee development initiatives with official health care providers on vaccine- avenues for regular training and skill development preventable illnesses, newer vaccines, • Implementation of collaborative planning, communication skills and adverse events micro-plan development and service provision reporting at community level among frontline workers. • Poor coordination among different Members of community may be involved to cadres of field-based staff enhance development of collaborative and needs- responsive micro-plans Vaccine logistics • Centrally driven demand estimation • Rationalize demand estimation based on locally based on historical trends of inconsistent available facility- and community-based databases data • Regular mapping of cold-chain assets with • Poorly sustained cold-chain identification of non-functional units for repair/ maintenance replacement • Development of local (district/sub-district) funds for cold-chain repair and replacement EPI management • Poor record-keeping in EPI management • Establishment of district data-cells to conduct information system information system and limited regular sub-district surveys to obtain accurate utilization of submitted data for estimates of vaccine coverage decision-making • Rationalization and revision of paper based • Absence of feedback at district level for management information tools improving data quality • Adoption of mobile device-based technology for rapid service data collection • Rigorous and regular assessment of submitted service data, with timely feedback to improve and maintain data quality Poor community • No appreciable increase in vaccine • Development of evidence-based communication uptake of vaccinations uptake among illiterate and low-income packages focusing on service uptake among segments of society different segments of society, e.g. rural populations • Poor communication skills of health and people with low literacy care providers and high rate of missed • Regular training of health care providers to enhance opportunities technical knowledge, communication skills and • Cultural and religious myths propagated staff attitudes regarding vaccination services by influential community leaders to • Provision of effective communication materials for prevent uptake of vaccination use by health care providers and for distribution among parents • Engagement of community and religious leaders to lend public support to religious instruction activities in the local context • Introduction of EPI services in health facilities where they are currently not offered • Visible, well-lit signboards identifying EPI centres at health care facilities and conveying information about the centre and services provided EPI = expanded programme on immunization; GIS = geographic information system.

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Discussion and policy monitoring of EPI activities (57,58). allowing efficient management of scarce recommendations Provincial and national comprehensive resources (59). Bottlenecks in vaccine multi-year plans have been developed delivery and storage must be identified, With close to 4 in 10 children in Pakistan after much deliberation and consensus and sustainable solutions developed, not fully immunized in their first year of building. These plans need to be vigor- for ensuring uninterrupted vaccine sup- life (43), urgent attention needs to be ously followed up and implemented plies at local levels. paid to service delivery and demand for to improve EPI performance through Demand creation through regu- vaccination among the general public. collaborative action. lar reminders, mass communication Although devolution of health services Level-specific training should be programmes and grassroots level en- has afforded considerable policy and developed and institutionalized to gagement are essential to combat com- resource space for improved perfor- improve managerial skills among EPI munity misperceptions and to increase mance of the local health care systems, management tiers and service provid- acceptance of vaccination services (60). entrenched systemic bottlenecks need ers, and poor structures of governance Despite engagement of the not-for- to be identified, scientifically evaluated must be addressed through institutional profit sector in advocacy and promo- and addressed to achieve sustainable strengthening and improved monitor- tion at grassroots levels, their impact on improvements in programme perfor- ing and accountability of concerned vaccination uptake is yet to be studied mance. While generic recommenda- cadres of managers and frontline work- (61). Consequently, these well-placed tions can be made, these need to be ers. institutions remain undirected by rel- contextualized given variable interpro- Coverage of vaccination services evant research, thus failing to capitalize vincial and inter-district performance can be improved through rational rede- on the significant potential for change. (22). Besides initiating immediate steps ployment of vaccinators and task-shift- It is imperative that work conducted by to improve vaccination services, it is ing involving training and deployment these organizations be mapped and sys- essential to identify and rectify strategic of additional community-based service tematically evaluated to assess their rel- factors affecting uptake of vaccination providers, e.g. lady health workers and evance and enhance their contribution services, including health-seeking be- community midwives for immunizing to the pool of immunization-focused haviour, community-based perceptions children within their catchment areas, activities within Pakistan (62). regarding vaccines and women’s educa- leaving vaccinators to focus on areas not It is through immediate, compre- tion and autonomy (49,53,56). The covered by allied workers. hensive and data-driven planning and specific recommendations are sum- Outdated and inaccurate systems sustained action that the languishing marized in Table 3. Briefly, in the post- of data collection and collation need re- rates of routine immunization in Paki- 18th-Amendment scenario, provincial view to improve the rigour and validity stan can be improved, leading in turn to EPI programmes in collaboration with of collected data. Adaptation of modern reductions in local and regional mortal- departments of health, district govern- technology, including mobile-device ity rates and the achievement of long- ments and implementation partners supported health initiatives to reduce term improvements in the health of the should develop a renewed scope of work workload must be considered for rapid country’s children. for each tier of programme functioning, data collection, making data-based Funding: None. with procedures for accountability and decision-making faster and easier and Competing interests: None declared.

References

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Re- perience of devolution in district health system of Pakistan: search and Development Solutions Policy Briefs Series No. perspectives regarding needed reforms. J Pak Med Assoc. 2012 3. Washington (DC): United States Agency for International Jan;62(1):28–32. PMID:22352097 Development; 2013 (http://resdev.org/files/policy_brief/3/3. 38. Comprehensive multiyear plan. Immunization program of pdf, accessed 9 February 2016). Sindh province. Islamabad, Pakistan: Expanded Programme 21. Khowaja AR, Zaman U, Feroze A, Rizvi A, Zaidi AKM, Routine on Immunization; 2014 (http://epi.gov.pk/wp-content/up- EPI coverage: sub-district inequalities and reasons for immu- loads/2014/09/SIN.pdf, accessed 9 February 2016). nization failure in a rural setting in Pakistan. Asia Pac J Public 39. Comprehensive multiyear plan: immunization program of Bal- Health. 2015 Mar;27(2):NP1050-9. PMID:22186395 uchistan province. Islamabad, Pakistan: Expanded Programme 22. Cockcroft A, Andersson N, Omer K, Ansari NM, Khan A, on Immunization; 2014 (http://epi.gov.pk/wp-content/up- Chaudhry UU, et al. One size does not fit all: local determinants loads/2014/09/BAL.pdf, accessed 9 February 2016). of measles vaccination in four districts of Pakistan. BMC Int 40. Comprehensive multiyear plan: immunization program of Health Hum Rights. 2009 Oct 14;9 Suppl 1:S4. PMID:19828062 FATA. Islamabad, Pakistan: Expanded Programme on Immu- 23. Pakistan Demographic and Health Survey, 1990/1991. Colum- nization, 2014. bia (MD): IRD/Macro International Inc. and Pakistan National 41. Mushtaq MU, Shahid U, Majrooh MA, Shad MA, Siddiqui AM, Institute of Population Studies; 1992 (http://dhsprogram. Akram J. From their own perspective-constraints in the polio com/pubs/pdf/FR29/FR29.pdf, accessed 9 February 2016). eradication initiative: perceptions of health workers and man- 24. Pakistan Demographic and Health Survey 2006–07. Calverton agers in a district of Pakistan’s Punjab province. BMC Int Health (MD): Macro International Inc. and Pakistan National Institute Hum Rights. 2010;10(22):22. PMID:20731832 of Population Studies; 2008 (https://dhsprogram.com/pubs/ 42. Shaikh BT, Hafeez A. Strengthening health system with key strat- pdf/FR200/FR200.pdf, accessed 9 February 2016).. egies in the post devolution times in Pakistan. Position Paper 25. Usman HR, Kristensen S, Rahbar MH, Vermund SH, Habib F, Series No. 2. Islamabad, Pakistan: Health Services Academy; Chamot E. Determinants of third dose of diphtheria-tetanus- 2012 (http://hsa.edu.pk/aboutus/hsa-pub/position-papers/

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HSA%20Position%20paper%20No%202-Strengthening%20 52. Favin M, Steinglass R, Fields R, Banerjee K, Sawhney M. Why health%20system%20%281%29.pdf, accessed 9 February children are not vaccinated: a review of the grey literature. Int 2016). Health. 2012 Dec;4(4):229–38. PMID:24029668 43. Shah F, Bashir-ul-Haq M, Navaratne KV, Inaam-ul-Haq TM. 53. Lambo JA, Nagulesapillai T. Neonatal tetanus elimination Kostermans K, Presthus G, et al. Situation analysis: new vaccine in Pakistan: progress and challenges. Int J Infect Dis. 2012 introduction in an under-performing programme-a dilemma Dec;16(12):e833–42. PMID:22940280 for Pakistan. J Pak Med Assoc. 2013;63(8):997–1002. 54. Andersson N, Cockcroft A, Ansari NM, Omer K, Baloch M, Ho 44. Sheikh SS, Ali SA. Predictors of vaccination card retention in Foster A, et al. Evidence-based discussion increases childhood children 12–59 months old in Karachi, Pakistan. Oman Med J. vaccination uptake: a randomised cluster controlled trial of 2014 May;29(3):190–3. PMID:24936268 knowledge translation in Pakistan. BMC Int Health Hum Rights. 45. Health facility assessment. Sindh provincial report. Lahore: 2009;9 Suppl 1:S8. PMID:19828066 Technical Resource Facility; 2012 (http://www.trfpakistan.org/ 55. Warraich HJ. Religious opposition to polio vaccination. Emerg LinkClick.aspx?fileticket=DVWqxBDJs6s%3D&tabid=2618, ac- Infect Dis. 2009 Jun;15(6):978. PMID:19523311 cessed 9 February 2016). 56. Wado YD, Afework MF, Hindin MJ. Childhood vaccination 46. Cold chain inventory system in selected districts of Pakistan in rural southwestern Ethiopia: the nexus with demographic (preliminary analysis report). Islamabad, Pakistan: United Na- factors and women's autonomy. Pan Afr Med J. 2014 Jan 18;17 tions Children’s Fund; 2014. Suppl 1:9.PMID:24624243 47. Coverage evaluation survey expanded program on immuniza- 57. Schwartz JB, Bhushan I. Improving immunization equity tion. Islamabad, Pakistan: Ministry of Health: 2006. through a public-private partnership in Cambodia. Bull World Health Organ. 2004 Sep;82(9):661–7. PMID:15628203 48. Bugvi AS, Rahat R, Zakar R, Zakar MZ, Fischer F, Nasrullah M, et al. Factors associated with non-utilization of child im- 58. Levin A, Kaddar M. Role of the private sector in the provision of munization in Pakistan: evidence from the Demographic and immunization services in low- and middle-income countries. Health Survey 2006–07. BMC Public Health. 2014;14(232):232. Health Policy Plan. 2011 Jul;26 Suppl 1:i4–12. PMID:21729916 PMID:24602264 59. Teng JE, Thomson DR, Lascher JS, Raymond M, Ivers LC. Using 49. Owais A, Hanif B, Siddiqui AR, Agha A, Zaidi AK. Does improv- Mobile Health (mHealth) and geospatial mapping technology ing maternal knowledge of vaccines impact infant immuni- in a mass campaign for reactive oral cholera vaccination in rural zation rates? A community-based randomized-controlled Haiti. PLoS Negl Trop Dis. 2014;8(7):e3050. PMID:25078790 trial in Karachi, Pakistan. BMC Public Health. 2011;11(239):239. 60. Oyo-Ita A, Nwachukwu CE, Oringanje C, Meremikwu MM. PMID:21496343 Interventions for improving coverage of child immunization in 50. Usman HR, Akhtar S, Habib F, Jehan I. Redesigned immunization low- and middle-income countries. Cochrane Database Syst card and center-based education to reduce childhood immu- Rev. 2011; (7):CD008145. PMID:21735423 nization dropouts in urban Pakistan: a randomized controlled 61. Zaidi A, Khan A. Evaluation of GAVI support to civil society trial. Vaccine. 2009 Jan 14;27(3):467–72. PMID:18996423 organisations. Country evaluation report: Pakistan. Islamabad, 51. Zaidi SM, Khowaja S, Kumar Dharma V, Khan AJ, Chandir S. Pakistan: GAVI Alliance: 2012. Coverage, timeliness, and determinants of immunization com- 62. Suryadevara M, Bonville CA, Ferraioli F, Domachowske JB. pletion in Pakistan: evidence from the Demographic and Health Community-centered education improves vaccination rates Survey (2006–07). Hum Vaccin Immunother. 2014;10(6):12– in children from low-income households. Pediatrics. 2013 20.PMID:24784118 Aug;132(2):319–25. PMID:23837177

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Short communication Responding to physical and psychological health impacts of disasters: case study of the Iranian disaster rehabilitation plan A. Ardalan,1,2,3 S. Sohrabizadeh,4 M.F. Latifi,5 M.H. Rajaei,2 A. Asadi,6 S. Mirbeigi,7 N. Rouhi 8 and H. Yousefi 2

التصدي لآلثار الصحية - البدنية والنفسية - للكوارث: دراسة حالة خلطة التأهيل اإليرانية ًاستعدادا للكوارث عل أردالن، ساناز سهرايب زاده، حممد فريد لطيفي، حممد حسني رجائي، عل أسدي، شبنم مريبيكي، نرجس روحي، مها يوسفي اخلالصــة:تصــف هــذه الورقــة طريقــة وضــع خطــة وطنيــة مســبقة ملواجهــة الكــوارث يف جمــال التأهيــل الصحــي - البــدين والنفــي - للمجتمعــات املنكوبــة. فالبيانــات التــي ُجعــت مــن مراجعــة لألدبيــات ومــن مناقشــات فريــق مــن اخلــرباء ســامهت يف عمليــة وضــع تعاريــف موحــدة للتأهيــل الصحــي البــدين والنفــي، ويف إنجــاز حتليــات األطــراف املعنيــة وSTEEP-V، ويف حتديــد املنظمــة املســؤولة عــن كل مهمــة واملنظــات املتعاونــة معهــا. وتــم اختيــار وزارة الصحــة ومنظمــة الرعايــة االجتمعيــة عــى أهنــا املنظمتــان املســؤولتان. ُواعتــربت اإلدارة املتكاملــة عــى جيــع املســتويات، وتبــادل املعلومــات، والتثقيــف، والتمويــل، ســب ًل لتحســني مشــاركة األطــراف املعنيــة وتعاوهنــا. هنــاك حاجــة إىل منظومــة ِّتقيــم مــدى تنفيــذ خطــة التأهيــل ملواجهــة الكــوارث باســتخدام مــؤرشات صحيحــة وموثوقــة.

ABSTRACT This paper describes the process of developing a national pre-disaster plan for physical health and psychological rehabilitation of disaster-stricken communities. Data gathered from a literature review and expert panel discussions informed the process of drawing up unified definitions of physical and psychological health rehabilitation, carrying out stakeholder and STEEP-V analyses, and assigning the responsible organization and the collaborative organizations for each task. The Ministry of Health and the Welfare Organization were selected as the two responsible organizations. Integrated management at all levels, and sharing information, education and funding, were identified as ways to improve stakeholders’ participation and collaboration. A system is needed for evaluating the implementation of the disaster rehabilitation plan, using valid and reliable indicators.

Agir en réponse aux conséquences physiques et psychologiques des catastrophes naturelles : étude de cas du plan de relèvement post-catastrophe en Iran

RÉSUMÉ La présente étude décrit le processus d'élaboration d’un plan national de préparation aux catastrophes naturelles pour la santé physique et la réhabilitation psychologique des populations frappées par les catastrophes. Les données collectées à partir d’une analyse documentaire et de groupes de discussions d’experts ont permis la rédaction de définitions unifiées en matière de réhabilitation au plan de la santé physique et mentale, la conduite d’analyses des parties prenantes et d’analyses PEST(E)-V (politique, économique, sociologique, technologique et écologique, et questions liées aux valeurs), et l’attribution de chaque tâche à l’organisation responsable et aux organisations collaboratives. Le ministère de la Santé et l’Organisation de protection sociale ont été désignées comme les deux entités responsables. Une prise en charge intégrée à tous les niveaux, le partage de l’information, l’éducation et l’aide financière ont été identifiés comme les moyens de renforcer la participation et la collaboration des parties prenantes. L’établissement d’un système est requis pour évaluer la mise en œuvre du plan de relèvement post-catastrophe à l’appui d’indicateurs valables et fiables.

1School of Public Health, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran. 2National Institute of Health Research, Tehran University of Medical Sciences, Tehran, Islamic Republic of Iran. 3Harvard Humanitarian Initiative, Harvard University, Cambridge, Massachusetts, United States of America. 4School of Health, Safety and Environment, Shahid Beheshti University of Medical Sciences, Tehran, Islamic Republic of Iran. 5National Disaster Management Organization, Tehran, Islamic Republic of Iran (Correspondence to M.F. Latifi: [email protected]). 6Department of Mental Health, Ministry of Health, Tehran, Islamic Republic of Iran. 7Welfare Organization, Tehran, Islamic Republic of Iran. 8School of Health Management and Information Sciences, Iran University of Medical Sciences, Tehran, Islamic Republic of Iran. Received: 27/05/15; accepted: 07/02/16

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Introduction developing a comprehensive pre-disas- advisory and expert panels, with the par- ter plan for physical and psychological ticipation of all involved organizations Natural disasters impose a great burden health rehabilitation in disaster-stricken working in the field of disaster health on populations, causing death, injury communities in the Islamic Republic management. and psychological disorders and fractur- of Iran. The underlying purpose was to The stakeholder analysis was initi- ing social as well as physical structures assist health practitioners and managers ated by listing all related organizations (1). Although the impact of disasters to deal with natural disasters by ensur- that had a potential interest in and/or on humans is wide-ranging (2), physi- ing that their roles and responsibilities impact on post-disaster physical health cal and mental health problems of the were clearly defined. and psychological rehabilitation. The affected population are the immediate list was drawn up by the research team concern after natural disasters 3( ,4). via the advisory panels. This was fol- Rehabilitation—the actions taken to Methods lowed by rating the organizations’ levels provide support for the well-being of of interest and of impact from 1 to 5 survivors in the aftermath of a disas- The rehabilitation plan was drawn up (positive to negative). This was carried ter—focuses on enabling people to re- with the participation of 80 experts out by representatives of the involved sume normal patterns of life (5). Clearly, working in 34 governmental and non- organizations at consensus meetings the speed and success of rehabilitation governmental organizations working and expert panels, and the data were is greatly enhanced when plans are in in the field of disaster health manage- analysed by the research team. Higher place prior to natural disasters to pro- ment. The Iranian National Disaster scores represented higher levels of inter- vide a framework for stakeholders to Management Organization drew up the est or impact. plan and supervised the project process. cope with the evolving conditions (6). The STEEP-V analysis was begun The project was handled by a research Some studies have highlighted the ne- by brainstorming participants on factors team who worked in the Department of cessity of planning for the restoration of that might have an influence on public Disaster and Emergency Health, at the people’s health and a few have reported policies, values, goals and strategies for National Institute of Health Research, on rehabilitation planning for restoring physical health and psychological reha- Tehran. The research team carried out the physical and mental health of dam- bilitation in either a favourable or unfa- the literature review, data gathering and aged people (7–11). To our knowledge, vourable manner. At this stage, a subset analysis and facilitated at expert panels, however, no previously published paper of experts working in 34 governmental brainstorming and group discussions. has reported a pre-disaster rehabilita- and non-governmental organizations tion plan. The phases of establishing the plan participated through advisory and ex- The Islamic Republic of Iran is a were as follows. First, a comprehen- pert panels. sive literature review was made and highly disaster-prone country; during Expert panels, brainstorming and expert discussions were carried out to recent decades, disasters of different group discussions were the main meth- finalize unified, acceptable definitions kinds have affected about 42 million ods of data gathering. Experts from of physical health and psychological Iranians and killed 78 000 of them relevant disciplines-disaster epidemiol- rehabilitation that would be applied by (12,13). More attention is therefore ogy, disaster and emergency medicine, all involved organizations. Secondly, needed to planning for physical and rehabilitation management, and social a stakeholder analysis and STEEP-V psychological health rehabilitation of welfare-were invited to join the panel [social, technological, economic, en- affected people. Although some studies, discussions. In total, more than 20 ad- vironmental/ecological, political and carried out after the Bam earthquake visory and expert panels were held with value-based issues] analysis were in 2003, highlighted the mental and the contribution of 15–30 experts per made to establish the factors that will physical health problems and effective session. therapeutic interventions (14–16), no influence the Islamic Republic of Iran’s pre-disaster rehabilitation plans were post-disaster physical and mental health in place. Furthermore, while there are a rehabilitation up to 2024. The third step Results plethora of organizations to assist health was to ascertain the values, goals, objec- agencies in the rehabilitation process, tives and strategies of the plan. Finally, Physical health and no national plans have been drawn up the main responsible organizations and psychological rehabilitation to manage the organizations involved the relevant collaborative organizations plan after disasters and to avoid any duplica- as well as their responsibilities and col- After the literature review and the tion of efforts. To fill these gaps, the laborative functions were identified stakeholders’ consensus, the follow- present paper reports on the process of according to the data extracted from ing definitions of physical health and

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psychological rehabilitation were ap- Table 1 Analysis of stakeholders’ levels of interest and impact on post-disaster proved: physical and psychological health rehabilitation in the Islamic Republic of Iran Stakeholder/group Level of Level of • Physical rehabilitation: supportive in- interesta impacta terventions and services provided for Ministry of Health +5 +5 people with physical disability caused Community health workers +5 +5 by the disaster to help them cope with this special situation and act as National Disaster Management Organization— health team +5 +3 productive individuals in their com- National Disaster Management Organization— munities. relief, rescue and public education team +5 +3 • Psychological rehabilitation: psy- Iranian Red Crescent Society +5 +3 chological supportive care and in- Iranian Blood Transfusion Organization +5 +3 terventions provided after mental University of Social Welfare and Rehabilitation trauma resulting from disasters. Ser- Sciences +5 +2 vices would be provided for shocked Vulnerable groups and affected people +5 +1 and damaged people, providers and For-profit nongovernmental organizations +5 +1 disaster managers in the short, me- Humanitarian associations supporting dium and long term. rehabilitation services +5 +1 According to the stakeholder Welfare Organization +4 +5 analysis, the following organizations Providers of health care, rehabilitation and social and stakeholders had the highest in- services +4 +5 terest in post-disaster physical health World Health Organization +4 +5 and psychological rehabilitation: the Passive Defence Organization +4 +5 health workgroup of the National Dis- World Bank +4 +3 aster Management Organization (a Social Work Association +4 +3 governmental organization for manag- Non-profit organizations +4 +2 ing disasters at the national and local levels); the relief, rescue and public Consultant clinics +4 +2 education team of the National Disas- Basij Medical Association +3 +5 ter Management Organization; Min- Nursing Organization of Iran +3 +3 istry of Health; Iranian Red Crescent Psychological Organization of Iran +3 +2 Society; University of Social Welfare United Nations Children’s Fund +3 +2 and Rehabilitation Sciences; Iranian Central bank and other banks +3 +2 Blood Transfusion Organization; for- Central Insurance Organization +3 +2 profit nongovernmental organizations; Iranian Medical Council +2 +3 vulnerable groups and affected peo- aNumbers show the strength of trends and signs show the trend direction. ple; and community health workers (behvarzan). The stakeholders with the highest impact on physical health information, education and funding rehabilitation plan and services had the and psychological rehabilitation were were identified as the best methods of highest positive score in the techno- identified as the Ministry of Health; improving stakeholders’ participation logical category, while inadequate basic Welfare Organization (a governmental and collaboration. services with unqualified staffing had organization responsible for provid- The most important factors re- the greatest negative score. In addition, ing a healthy life for poor and disabled vealed by STEEP-V analysis are shown population vulnerability was identified people); World Health Organization; in Table 2. Such social, technical, eco- as the strongest negative factor in the so- Basij Medical Association (a private nomic, environmental, political and cial group. Policy-making and planning association of medical experts); Pas- value-based issues will affect the whole for disaster rehabilitation, and training sive Defence Organization (a private operation of the physical health and responsible human resources, had the organization managed by the armed psychological rehabilitation plan up to highest positive ratings in the political forces to provide the national security the year 2024; the STEEP-V factors and value-based category. in pre- and post-disaster phases); and will be reviewed and updated after 10 The policies of physical and psycho- providers of health care, rehabilitation years. For example, the media’s role in logical health rehabilitation were defined and social services (Table 1). Sharing keeping people informed about the as follows: integrated rehabilitation

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management at all levels; knowledge Table 2 STEEP-V analysis of the social, technological, environmental, economic, management based on scientific evi- political and value-based factors that will impact on the Islamic Republic of Iran’s dence and local technology; use of re- post-disaster physical health and psychological rehabilitation up to 2024 ligious associations and institutions for Factors Strength and trend directiona facilitating rehabilitation efforts; a focus Social factors on vulnerable groups such as children and elderly and disabled people; com- Public demands for rehabilitation services +2 munity-based rehabilitation planning; Public knowledge about available services +1 and comprehensive physical health and Numbers of affected people +1 psychological rehabilitation in line with Drug dependency –2 sustainable development. The values Negative attitudes of people to the quality of which should be followed by all respon- rehabilitation services –4 sible and collaborative organizations Lack of community partnership –4 were described as: to consider human Lack of social capital –4 dignity; to focus on equality in all the Vulnerability of the population –5 stages; to act in line with national values Political and value-based factors and autonomy; and to take into account Rehabilitation policies and plans +5 the concepts and values of Islam. Training responsible human resources +5 Religious associations and institutions for facilitating Goals, strategies and rehabilitation efforts +5 responsible and collaborative Reinforcement and improvement of mental health plans +3 organizations Lack of focus on equality, human dignity and quality of life –2 The goals and strategies of physical Lack of punctuality and flexibility in providing health and psychological rehabilitation rehabilitation services –2 and the responsible and collaborative Lack of a teamwork culture and multi-disciplinary organizations were identified in ac- collaboration –3 cordance with the policies and values Foreign threats and sanctions –4 defined above, as well as the stakeholder Lack of coordination and management –4 analysis and STEEP-V outputs. Technological factors Physical health rehabilitation Media role in keeping people informed about the rehabilitation plan and services +5 Goal: rapid and effective restoration of Availability of information technology +3 physical capabilities of people disabled by disasters, as well as those with pre- Capacity of rehabilitation services +3 existing disabilities, to allow them to Knowledge management +2 perform routine activities of life inde- Public health indicators +2 pendently. Research and educational technology +2 Strategies: standardization of physi- Man-made hazards –3 cal rehabilitation services; development Inadequate basic services and unqualified staffing –3 of technical, financial and human re- Environmental and economic factors sources to provide the necessary ser- Resource allocation related to rehabilitation +1 vices; and establishment of networks for Islamic Republic of Iran’s natural hazard profile –2 physical rehabilitation services. Disaster vulnerability in the involved organizations –2 Responsible organization: Ministry of Inadequate social/disaster insurance and financial Health. institutions –3 Low economic status of the population –4 Collaborative organizations: Welfare Lack of investments and participation of private sectors for Organization, Iranian Red Crescent providing rehabilitation services –4 Society, Social Security Organization Unemployment status –4 and Basij Medical Association. Lack of financial savings to cope with disasters –5 Psychological health rehabilitation Social vulnerability and unequal development –5 Goal: to prevent and treat psychological aNumbers show the strength of trends and signs show the trend direction. disorders resulting from natural disasters

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Table 3 Outline of the Iranian physical health and psychological rehabilitation plan: the most important tasks of responsible organizations before and after disasters Domain/organization Pre-disaster tasks Post-disaster tasks Physical health rehabilitation Responsible organization: Developing preparedness action plan Developing a comprehensive database Ministry of Health for post-disaster physical rehabilitation, of post-disaster disabled victims and the including preparing a pre-disaster list of resources required for meeting their needs people with different kinds of disabilities

Carrying out needs and capacity Providing different kinds of physical assessments of Ministry of Health rehabilitation services for disaster-affected services and staff involved in providing people post-disaster physical rehabilitation services

Capacity-building of physical Delivering community-based services, rehabilitation specialists (educating and with a focus on developing the capacities training) of affected populations

Continuous planning for long-term Continuing delivery of physical physical rehabilitation in disaster- rehabilitation services to disabled damaged health centres individuals after disasters (supporting and training)

Planning for supplying facilities as well Participating in management of as developing infrastructure for post- humanitarian aid related to physical disaster physical health rehabilitation rehabilitation

Capacity-building of specialized Monitoring and evaluating physical nongovernmental organizations for rehabilitation services delivering physical rehabilitation services after disasters

Psychological rehabilitation Responsible organization: Developing preparedness action Providing various types of psychological Welfare Organization plan for post-disaster psychological rehabilitation services for disaster-affected rehabilitation, including preparing a pre- people, including developing a database disaster list of people with mental health for recording cases of post-disaster mental disorders health disorders Developing guidelines and standards for Continuing revision of the action plan psychological rehabilitation services based on available resources and the changing status of damaged areas Participating in the capacity Identifying substance abusers and development of professional providing mental health services for them nongovernmental organizations Supporting research required for Providing mental health services for rescue improvement of psychological and relief workers, disaster managers and rehabilitation other aid providers Informing the community about the Providing virtual mental health services by psychological consequences of disasters means of 24-hour phone lines and online and the related rehabilitation services web pages Providing regular, evidence-based Monitoring and evaluating psychological training for psychologists and social rehabilitation services workers

in order to restore the mental health of other social factors; to integrate mental disabled and poor people in the Islamic people adversely affected by disasters. health interventions into relief efforts; Republic of Iran). Strategies: to establish psychological and to encourage positive thinking Collaborative organizations: Min- rehabilitation services; to develop and among the affected communities. istry of Health, Iranian Red Crescent organize public/professional human Responsible organization: Welfare Or- Society, Social Security Organization, resources; to provide standard psycho- ganization (an important public organi- Psychological Organization and Basij logical services based on gender and zation with the mission of supporting Medical Association.

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The final part of the report sum- definitions for physical health and psy- It is recommended that a system be marized the most important tasks of the chological rehabilitation in order to developed for evaluating the implemen- responsible organizations (Table 3). avoiding misunderstandings during tation of the physical health and psycho- the rehabilitation phase. Based on the logical rehabilitation plan, using valid stakeholder and STEEP-V analyses, and reliable indicators. Additionally, the Discussion community health workers (behvar- findings suggest that an executive guar- zan) had the highest score in both antee, for example from the Office of the The present project represents the interest and impact on rehabilitation President of the Islamic Republic of Iran, first attempt to develop a pre-disaster initiatives. It seems that the capacity of should be made to enforce the involved physical health and psychological public health centres is important for ef- organizations to fulfil their responsibili- rehabilitation plan for the Islamic Re- fective implementation of the physical ties before and after disasters. The plan public of Iran. Some studies have re- health and psychological rehabilitation was focused on natural disasters and ported rehabilitation plans developed plan. However, such capacity has not further research will be required to make after a disaster 12( ,13). Although these so far been applied for post-disaster a comprehensive response and rehabili- post-disasters plans may be success- tation plan for man-made and bioterror- physical health and psychological reha- ful, planning for physical and mental ism emergencies. health rehabilitation is more effective bilitation efforts in the Islamic Republic if it is done before the occurrence of a of Iran. disaster (6). A number of studies have Pre-defined tasks of the respon- Acknowledgements highlighted the necessity of develop- sible organizations and collaborative ing a pre-disaster rehabilitation plan organizations can help them to work The project was conducted by De- for the physical and mental health of in a more coordinated way. These partment of Disaster and Emergency affected people (7–11). However, responsibilities were determined and Health, National Institute of Health such a plan should be in line with the approved by all the involved organi- Research in Tehran. The authors grate- sociocultural context of the affected zations in order to avoid any duplica- fully acknowledge the participation of communities and the structure of the tion of efforts after disasters. Social all involved organizations and stake- available disaster health management protection and financial support for holders during planning process. organizations. vulnerable people, including children Funding: The plan was financially sup- The national rehabilitation plan for and disabled and elderly persons ported by the National Disaster Man- the Islamic Republic of Iran included were also considered in the public agement Organization. providing unified terminology and policy. Competing interests: None declared.

References

1. Beaudoin CE. News, social capital and health in the context of org/assets/tools_guidelines/predisaster_planning/US%20 Katrina. J Health Care Poor Underserved. 2007 May;18(2):418– National%20Disaster%20Recovery%20Frameworkv2.pdf, ac- 30. PMID:17483569 cessed 26 February 2016). 2. Guidance note on recovery: health. Geneva: United Nations 7. Gosney J, Reinhardt JD, Haig AJ, Li J. Developing post- Development Programme/International Recovery Platform/ disaster physical rehabilitation: role of the World Health United Nations Office for Disaster Risk Reduction; 2010 Organization Liaison Sub-Committee on Rehabilitation Dis- (http://www.unisdr.org/files/18782_irphealth.pdf, accessed aster Relief of the International Society of Physical and Reha- 28 February 2016). bilitation Medicine. J Rehabil Med. 2011 Nov;43(11):965–8. PMID:22031340 3. Rauch A, Baumberger M, Moise F-G, von Elm E, Reinhardt JD. Rehabilitation needs assessment in persons with spinal cord 8. Heimann P, Issakov A. Repair and recovery of health systems: injury following the 2010 earthquake in Haiti: a pilot study us- WHO tools for evidence-based resource planning within the ing an ICF-based tool. J Rehabil Med. 2011 Nov;43(11):969–75. context of post-tsunami rehabilitation of health facilities and restoration of health services Geneva: World Health Organiza- PMID:22031341 tion; 2005. 4. Ciottone GR, editor. Disaster medicine. 3rd ed. Philadelphia: 9. Chowdhury M. Research report on a comparative study of Mosby Elsevier; 2006. disaster risk reduction and post disaster livelihood recovery 5. Aysan Y, Davis I. Rehabilitation and reconstruction. Geneva: program in Japan and Bangladesh. Kobe, Japan: Asian Disaster United Nations Development Programme/Department of Reduction Center; 2012. Humanitarian Affairs Disaster Management Training Pro- 10. Pakistan floods 2010. Early recovery plan for the health sec- gramme; 1993. tor. Islamabad: World Health Organization Health Clus- 6. National disaster recovery framework: strengthening disaster ter—Pakistan; 2011 (http://www.who.int/hac/crises/pak/ recovery for the nation. Washington (DC): Federal Emergency pakistan_early_recovery_plan_12february2011.pdf, accessed Management Agency; 2011 (http://www.recoveryplatform. 28 February 2016).

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11. Post-disaster rehabilitation activities in India [Internet]. New 14. Farhoudian A, Sharifi V, Rahimi A, Radgudarzi R, Mohammadi Delhi, India: Aga Khan Development Network; 2001 (http:// M, Yunesian M. The study of PTSD prevalence and its symp- www.akdn.org/india_rehabilitation.asp, accessed 28 February toms in affected people of Bam earthquake. Journal of Cogni- 2016). tive Sciences News. 2006;8(3):58–70. 12. Islamic Republic of Iran: disaster and risk profile. Basic country 15. Ghomashchi F. The effect of problem solving education on statistics and indicators [Internet]. Geneva: United Nations In- treatment of PTSD patients of Bam earthquake. Journal of ternational Strategy for Disaster Reduction; 2011 (http://www. Ardebil University of Medical Sciences. 2008;8(3):294–300. preventionweb.net/english/countries/statistics/?cid=81, ac- 16. Rahimi A, Farhoudian A, Radgudarzi R, Sharifi V, Yunesian M, cessed 28 February 2016). Mohammadi M. Revalence and change of drug use in affected 13. Moaierinezhad H. [The most destructive earthquakes of Iran]. people of Bam earthquake. Payesh Journal. 2006;6(3):209–17. Tehran: Khabar Online; 2012 (http://www.khabaronline.ir/ detail/235750/society/urban, accessed 28 February 2016).

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Short communication Environmental carcinogen exposure and lifestyle factors affecting cancer risk in Qatar: findings from a qualitative review R. Denholm,1 J. Schüz,1 K. Straif,2 F.M.H. Ali,3 F. Bonas,3 O. Gjebrea,3 C. Sifton 3 and A.C. Olsson 1

التعرض البيئي للمرسطنات ُوعوامل نمط احلياة التي تؤثر عل خماطر اإلصابة بالرسطان يف قطر: نتائج استعراض كيفي راشيل دهنومل، جوشيم شوتز، كريت ستيف، فالح حممد حسني عل، فيونا بوناس، أورسيدا جربيا، كليوي سيفتون، آن أولسون اخلالصــة:لتحقيــق األهــداف الصحيــة يف البــاد لألعــوام 2011- 2016أجــري اســتعراض كيفــي للتعــرض لعوامــل خطــر اإلصابــة بالرسطــان يف قطــر يف عــام . 2013 وشــملاالســتعراض التعــرض للعوامــلالبيئيــة املرسطنــة للبــرش )الوكالــة الدوليــة للبحــوث املتعلقــة بتصنيــف الرسطــان(، إضافــة إىل عوامــل نمــط احليــاة املعــروف أهنــا تؤثــر عــى خماطــر اإلصابــة بالرسطــان. وتــم جتميــع املعلومــات مــن جيــع املصــادر املتاحــة ُواســتعراضها. فكانــت املســتويات املذكــورة للجســيمتيف قطــر يف احلــد األعــى مللوثــات اهلــواء املحيــط التــي ذكــرت عــى الصعيــد الــدويل، وربــا تؤثــر مســتقب ً لعــى عــبء رسطــان الرئــة يف البــاد. وتشــري البيانــات املحــدودة عــن التعــرض املهنــي إىل أن أكــرب املخاطــر التــي تواجــه العاملــني يف صناعــة البنــاء والتشــييد يرجــح أن تكــون ناجــة عــن الغبــار البيئــي ومــا يتصــل بــه مــن ملوثــات اهلــواء. وأكــرب خماطــر اإلصابــة بالرسطــان بالنســبة للمواطنــني القطريــ نيقــد تكــون عوامــل نمــط احليــاة، ال ّســيم الســمنة واخلمــول البــدين وتعاطــي التبــغ. يــوىص بإجــراء مراقبــة موســعة لتكيــب ملوثــات اهلــواء ولتعــرض البــرش هلــا.

ABSTRACT To meet the country’s health goals for 2011–2016, a qualitative review of exposure to risk factors for cancer in Qatar was conducted in 2013. The review included exposure to environmental agents carcinogenic to humans (International Agency for Research on Cancer classification), as well as lifestyle factors known to affect cancer risk. Information from all available sources was assembled and reviewed. The levels of particulate matter reported in Qatar were in the upper range of ambient air pollutants reported internationally, and may influence the country’s future lung cancer burden. The limited data on occupational exposure suggests that the greatest risks for workers in the construction industry are likely to be from environmental dust and related air pollutants. The greatest cancer risks for Qatari nationals may be lifestyle factors, particularly obesity, physical inactivity and tobacco use. Extended monitoring of the composition of and human exposure to air pollutants is recommended.

Exposition aux carcinogènes environnementaux et facteurs associés aux modes de vie augmentant le risque de cancer au Qatar : résultats d’une analyse qualitative

RÉSUMÉ Afin d’atteindre les objectifs de santé fixés par le pays pour 2011-2016, une analyse qualitative de l’exposition aux facteurs de risque de cancer au Qatar a été conduite en 2013. L’analyse incluait l'exposition aux agents environnementaux cancérogènes pour l’homme (classification du Centre international de recherche sur le cancer) ainsi que les facteurs liés au mode de vie connus pour augmenter le risque de cancer. Des informations ont été rassemblées à partir de toutes les sources disponibles et ont fait l'objet d'un examen. Les niveaux de particules rapportés au Qatar se situaient dans la fourchette haute des polluants atmosphériques ambiants au niveau mondial, ce qui pourrait influencer la charge future du cancer du poumon dans le pays. Le nombre limité de données sur l’exposition professionnelle suggère que les risques les plus importants pour les professionnels de l’industrie du bâtiment seraient liés à la poussière environnementale et aux polluants atmosphériques qu’elle contient. Les risques de cancer les plus élevés pour les Qatariens proviendraient de facteurs associés aux modes de vie, en particulier l’obésité, la sédentarité et le tabagisme. Un suivi accru de la composition des polluants atmosphériques et de l’exposition de l’homme à ces derniers est recommandé.

1Environment and Radiation Section; 2IARC Monographs Section, International Agency for Research on Cancer, Lyon, France (Correspondence to A.C. Olsson: [email protected]). 3Supreme Council of Health, Doha, Qatar. Received: 02/09/15; accepted: 22/02/16

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Introduction of Health of Qatar together with the carcinogens in outdoor air and engine International Agency for Research on exhausts); behavioural factors (e.g. Globally, overall cancer incidence Cancer (IARC) conducted a qualita- exposure to tobacco smoke; levels and mortality rates are increasing (1). tive review in 2013 of environmental of obesity and physical activity); oc- Environmental factors that are poten- risk factors for cancer in Qatar. The cupational measures (e.g. exposures tially preventable make an important initial scope of the review covered ex- to asbestos and crystalline silica); and contribution to the burden of cancer posure to chemicals and pollutants medical diagnostics (e.g. exposure to worldwide (2). These include factors classified by IARC as carcinogenic to X-rays and selected diseases). The defi- such as exposure to environmental air humans. It was later decided to include nitions of carcinogens were based on pollution, occupational exposure to a review of lifestyle factors that are the January 2013 list of agents classified carcinogenic compounds, and lifestyle known to influence cancer risk. The carcinogenic to humans (group 1) in factors such as dietary choices and ex- findings were compared with similar the IARC monographs programme posure to tobacco smoke. data from other regions of the world. (Table 2) (6). Selected lifestyle factors In Qatar, malignant neoplasms This paper presents the main findings that affect cancer risk were based on the were the leading cause of death in and discusses the challenges of de- IARC Handbooks of Cancer Preven- women and the sixth most frequent termining cancer risk attributable to tion, which provide evaluations of the cause of death in men in 2009 (3). environmental exposures in the Qatari cancer-preventive potential of agents A key recommendation of the Qatar population. and interventions; this series is intended national cancer strategy for the years to complement the IARC monographs 2011–16 was to carry out a review programme (6) and the European of environmental carcinogens in the Methods Code against Cancer, 4th edition (7,8). country (4). The country’s national The information was assembled and health strategy for the same period had Table 1 details the types of data col- reviewed from all available resources the explicit aim of developing national lected and the sources of data for the about the occurrence, monitoring and occupational health standards, policies overall review. Data were collected in legislation of carcinogenic exposures in and regulations and a monitoring sys- the following categories: food quality air, water and food sources and about tem (5). To inform and develop these (e.g. carcinogens found in food sam- lifestyle choices in Qatar. Collabora- important goals, the Supreme Council ples and bottled water); air quality (e.g. tors and stakeholders from relevant

Table 1 Sources of data for the qualitative review of environmental exposures to carcinogens in Qatar Type of data Source Data Carcinogens (IARC group 1 carcinogens)/lifestyle factors influencing cancer risk Food quality Central Food Laboratories, Routine data collection (random Aflatoxins; nitrate or nitrite; lead Supreme Council for Health sampling of imported food compounds; cadmium and items and bottled water from all cadmium compounds; arsenic ports of entry by the Qatar Port and inorganic compounds Authority section) 1999–2000, January to March 2013 Air quality Air Quality Department, Qatar Routine data collection from Outdoor air pollution (sulfur Ministry of Environment; WHO. three permanent air monitoring dioxide; nitrogen dioxide;

ambient (outdoor) air pollution stations since 2007; and one ozone; carbon monoxide); PM10

database, 2014 Global Health mobile station since 2008 and PM2.5 Observatory Traffic Department, Ministry of Routine data collection from Diesel engine exhaust Interior 2002 and 2012 Behavioural factors Public Health Department, World Health Organization Tobacco smoke, and second- Supreme Council for Health STEPwise report 2012, global hand tobacco smoke, weight adult tobacco survey 2013 control, physical activity Occupational Ministry of Labour and Social Labour force sample survey Selected exposures (asbestos, measures Affairs 2007, 2008, 2009 and 2011 crystalline silica) in the main industries according to CAREX) Medical diagnostics Hamad Medical Corporation Annual report 2011 Hepatitis B; hepatitis C; parasitic diseases; HIV/AIDS|; X-radiation

IARC = International Agency for Research on Cancer; CAREX = European carcinogen exposure database; PM10 = particulate matter 10 µm or less in diameter; PM2.5 = particulate matter 2.5 µm or less in diameter.

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Table 2 Agents classified carcinogenic to humans (group 1). Source: International Agency for Research on Cancer (IARC) monographs, volumes 1–105 (6) Agent Group IARC volume Year 1,3-butadiene 1 Sup 7, 54, 71, 97, 100F 2012

2,3,4,7,8-pentachlorodibenzofuran 1 100F 2012

2,3,7,8-tetrachlorodibenzo-para-dioxin 1 Sup 7, 69, 100F 2012

2-naphthylamine 1 4, Sup 7, 99, 100F 2012

3,4,5,3,4-pentachlorobiphenyl (PCB-126) 1 100F 2012

4,4-methylenebis(2-chloroaniline) (MOCA) 1 Sup 7, 57, 99, 100F 2012

4-aminobiphenyl 1 1, Sup 7, 99, 100F 2012

Clonorchis sinensis (infection with) 1 61, 100B 2012

Helicobacter pylori (infection with) 1 61, 100B 2012

N'-nitrosonornicotine (NNN) and 4-(N-nitrosomethylamino)-1-(3-pyridyl)- 1-butanone (NNK) 1 Sup 7, 89, 100E 2012

Opisthorchis viverrini (infection with) 1 61, 100B 2012

ortho-toluidine 1 Sup 7, 77, 99, 100F 2012

Schistosoma haematobium (infection with) 1 61, 100B 2012

Acetaldehyde associated with consumption of alcoholic beverages 1 100E 2012

Acid mists, strong inorganic 1 54, 100F 2012

Aflatoxins 1 56, 82, 100F, Sup 7 2012

Alcoholic beverages 1 44, 96, 100E 2012

Aluminium production 1 34, Sup 7, 92, 100F 2012

Areca nut 1 85, 100E 2012

Aristolochic acid 1 82, 100A 2012

Aristolochic acid, plants containing 1 82, 100A 2012

Arsenic and inorganic arsenic compounds 1 23, Sup 7, 100C 2012

Asbestos (all forms, including actinolite, amosite, anthophyllite, chrysotile, crocidolite, tremolite) 1 14, Sup 7, 100C 2012

Auramine production 1 Sup 7, 99, 100F 2012

Azathioprine 1 26, Sup 7, 100A 2012

Benzene 1 29, Sup 7. 100F 2012

Benzidine 1 29, Sup 7, 99, 100F 2012

Benzidine, dyes metabolized to 1 99, 100F 2012

Benzo[a]pyrene 1 Sup 7, 92, 100F 2012

Beryllium and beryllium compounds 1 Sup 7, 58, 100C 2012

Betel quid with tobacco 1 Sup 7, 85, 100E 2012

Betel quid without tobacco 1 Sup 7, 85, 100E 2012

Bis(chloromethyl)ether; chloromethyl methyl ether (technical-grade) 1 4, Sup 7, 100F 2012

Busulfan 1 4, Sup 7, 100A 2012

Cadmium and cadmium compounds 1 58, 100C 2012

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Table 2 Agents classified carcinogenic to humans (group 1). Source: International Agency for Research on Cancer (IARC) monographs, volumes 1–105 (6) (continued) Agent Group IARC volume Year Chlorambucil 1 26, Sup 7, 100A 2012

Chlornaphazine 1 4, Sup 7, 100A 2012

Chromium (VI) compounds 1 Sup 7, 49, 100C 2012

Coal gasification 1 Sup 7, 92, 100F 2012

Coal, indoor emissions from household combustion of 1 95, 100E 2012

Coal-tar distillation 1 92, 100F 2012

Coal-tar pitch 1 35, Sup 7, 100F 2012

Coke production 1 Sup 7, 92, 100F 2012

Cyclophosphamide 1 26, Sup 7, 100A 2012

Cyclosporine 1 50, 100A 2012

Diethylstilboestrol 1 21, Sup 7, 100A 2012

Engine exhaust, diesel 1 46, 105 2013

Epstein-Barr virus 1 70, 100B 2012

Erionite 1 42, Sup 7, 100C 2012

Oestrogen therapy, postmenopausal 1 72, 100A 2012

Oestrogen–progestogen menopausal therapy (combined) 1 72, 91, 100A 2012

Oestrogen–progestogen oral contraceptives (combined) 1 72, 91, 100A 2012

Ethanol in alcoholic beverages 1 96, 100E 2012

Ethylene oxide 1 Sup 7, 60, 97, 100F 2012

Etoposide 1 76, 100A 2012

Etoposide in combination with cisplatin and bleomycin 1 76, 100A 2012

Fission products, including strontium-90 1 100D 2012

Formaldehyde 1 Sup 7, 62, 88, 100F 2012

Haematite mining (underground) 1 1, Sup 7, 100D 2012

Hepatitis B virus (chronic infection with) 1 59, 100B 2012

Hepatitis C virus (chronic infection with) 1 59, 100B 2012

Human immunodeficiency virus type 1 (infection with) 1 67, 100B 2012

Human papillomavirus types 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59 1 64, 90, 100B 2012

Human T-cell lymphotropic virus type I 1 67, 100B 2012

Ionizing radiation (all types) 1 100D 2012

Iron and steel founding (occupational exposure during) 1 34, Sup 7, 100F 2012

Isopropyl alcohol manufacture using strong acids 1 Sup 7, 100F 2012

Kaposi sarcoma herpesvirus 1 70, 100B 2012

Leather dust 1 100C 2012

Magenta production 1 Sup 7, 57, 99, 100F 2012

Melphalan 1 9, Sup 7, 100A 2012

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Table 2 Agents classified carcinogenic to humans (group 1). Source: International Agency for Research on Cancer (IARC) monographs, volumes 1–105 (6) (continued) Agent Group IARC volume Year Methoxsalen (8-methoxypsoralen) plus ultraviolet A radiation 1 24, Sup 7, 100A 2012

Mineral oils, untreated or mildly treated 1 33, Sup 7, 100F 2012

MOPP and other combined chemotherapy including alkylating agents 1 Sup 7, 100A 2012

Neutron radiation 1 75, 100D 2012

Nickel compounds 1 Sup 7, 49, 100C 2012

Painter (occupational exposure as a) 1 47, 98, 100F 2012

Phenacetin 1 24, Sup 7, 100A 2012

Phenacetin, analgesic mixtures containing 1 Sup 7, 100A 2012

Phosphorus-32, as phosphate 1 78, 100D 2012

Plutonium 1 78, 100D 2012

Radioiodines, including iodine-131 1 78, 100D 2012

Radionuclides, alpha-particle-emitting, internally deposited 1 78, 100D 2012

Radionuclides, beta-particle-emitting, internally deposited 1 78, 100D 2012

Radium-224 and its decay products 1 78, 100D 2012

Radium-226 and its decay products 1 78, 100D 2012

Radium-228 and its decay products 1 78, 100D 2012

Radon-222 and its decay products 1 43, 78, 100D 2012

Rubber manufacturing industry 1 28, Sup 7, 100F 2012

Salted fish, Chinese-style 1 56, 100E 2012

Semustine [1-(2-Chloroethyl)-3-(4-methylcyclohexyl)-1-nitrosourea, 1 Sup 7, 100A 2012 Methyl-CCNU]

Shale oils 1 35, Sup 7, 100F 2012

Silica dust, crystalline, in the form of quartz or cristobalite 1 Sup 7, 68, 100C 2012

Solar radiation 1 55, 100D 2012

Soot (as found in occupational exposure of chimney sweeps) 1 35, Sup 7, 92, 100F 2012

Sulfur mustard 1 9, Sup 7, 100F 2012

Tamoxifen 1 66, 100A 2012

Thiotepa 1 Sup 7, 50, 100A 2012

Thorium-232 and its decay products 1 78, 100D 2012

Tobacco smoke, second-hand 1 83, 100E 2012

Tobacco smoking 1 83, 100E 2012

Tobacco, smokeless 1 Sup 7, 89, 100E 2012

Treosulfan 1 26, Sup 7, 100A 2012

Ultraviolet radiation (wavelengths 100–400 nm, encompassing UVA, UVB, 1 55, 100D 2012 and UVC)

Ultraviolet-emitting tanning devices 1 100D 2012

Vinyl chloride 1 Sup 7, 97, 100F 2012

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Table 2 Agents classified carcinogenic to humans (group 1). Source: International Agency for Research on Cancer (IARC) monographs, volumes 1–105 (6) (concluded) Agent Group IARC volume Year Wood dust 1 62, 100C 2012

X-radiation and gamma-radiation 1 75, 100D 2012

MOPP = mechlorethamine, oncovin, procarbazine, and prednisone.

government institutions and organiza- exposures to the main industries based the annual mean levels of particulate

tions were contacted for face-to-face on the European CAREX [carcinogen matter 10 µm or less in diameter (PM10) meetings, and data from routine sur- exposure] database (11,12). We also in the capital city, Doha, were 168 µg/ veillance and other unpublished infor- discuss the likelihood of the most im- m3, and for particulate matter 2.5 µm mation were collected when possible. portant exposures based on a review of or less in diameter (PM2.5) were 93 Data about air, water and food sources published reports, including informa- µg/m3 (14). Levels reported in Doha were obtained from the Government tion from Qatar. exceeded those from other large cities in of Qatar’s Central Food Laboratories, For comparison with other coun- the region such as Abu Dhabi and inter- Air Quality Department and Traffic tries and regions we collected data from nationally including Beijing (Figure 1). Department. An indication of X-ray comparable sources, including the Few studies have investigated air exposure and disease prevalences were World Health Organization (WHO) pollution composition in the region. obtained from Hamad Medical Cor- STEPwise approach to Surveillance The United States of America (USA) poration, a non-profit national health national reports (13) and WHO air enhanced particulate matter surveil- organization. Data on the prevalence pollution reports (14). of tobacco smoking, obesity and physi- lance programme conducted chemical cal inactivity were obtained from the and physical analysis of air pollution World Health Organization’s STEP- Results in USA army bases across the Middle wise report 2012 (9) and the Global East, including Al Udied, south-west of Adult Tobacco Survey 2013 (10). No Air pollution Doha (15,16). The programme showed specific data on occupational exposures Reported levels of air pollution in Qatar a PM10:PM2.5 mass ratio of 0.41, indicat-

were available to us, although we used are higher than those for other countries ing a high fraction of PM10 was com- the Labour Force Statistics Bulletin of in the Eastern Mediterranean Region posed of coarse dust in the air. High

the Qatar Ministry of Development (EMR) and some industrialized coun- concentrations of sulphate in PM2.5 Planning and Statistics and attributed tries elsewhere in the world. In 2012, were also found, most likely from sulfur

Annual mean PM2.5 µg/m3

London, UK

Paris, France

Mexico city, Mexico

Johannesburg, South Africa

Beijing, China

Abu Dhabi, United Arab Emirates

Doha, Qatar

Karachi, Pakistan

Delhi, India 0 20 40 60 80 100 120 140 160 180

Figure 1 Levels of particulate matter 2.5 µm or less in diameter (PM2.5) in selected cities for the last available year over the period 2008–2013. Source: World Health Organization ambient (outdoor) air pollution in cities database 2014 (14)

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dioxide emissions from petrochemi- BMI ≥ 30 kg/m2, while more women have investigated cancer risk associated cal and other industries. Overall, the compared with men were physically with exposure to particulate matter in report concluded that there was little inactive (54.2% and 37.4% respectively) arid settings, where a large proportion difference in the dust composition in (9). The overall prevalence of tobacco of the atmospheric particulate matter is Middle Eastern countries compared smoking in 2013 was 20.2% in men and expected to be sand particles from the with Djibouti, China and the USA. 3.1% in women aged 15+ years, with the land. Evidence from the enhanced par- proportion increasing to about 25% in ticulate matter surveillance programme Occupational exposures Qatari men aged 25+ years. Waterpipe indicate that the composition of par- Building construction is currently the tobacco was smoked by 3.4% of the ticulate matter in the Middle East is dominant industry in Qatar, employing population, a higher proportion of men comparable to that of other arid regions more than 568 000 workers in 2013 compared with women (4.9% and 1.6% (15,16). However, human exposure (17). The majority (99.7%) of construc- respectively) (10). to environmental air pollution is influ- tion workers are non-Qatari nationals, enced by meteorological factors and while most Qatari nationals are em- individual behaviour, such as the time ployed in the public administration and Discussion spent outdoors and individual levels defence sector (53.7%) (17). The main of activity, which are likely to be differ- type of aggregates used for concrete The original aim of this project was to ent in Qatar compared with countries constructions have changed from local provide a qualitative and quantitative of Europe and North America due to limestone to imported gabbro, a mafic review of the burden of cancer in Qatar the hot climate and social customs. Ex- igneous rock, containing less silica and attributable to different environmen- tended monitoring, including assessing more iron and magnesium compared tal and occupational carcinogens. concentrations of air pollutants and, in with quartz (18,19). The USA geo- The review was limited, however, to a particular, personal exposure monitor- logical survey show that countries of the qualitative assessment of cancer risk ing, is needed to better understand the Middle East have consumed relatively because quantitative data on exposures extent to which lung cancer risk esti- low levels of asbestos compared with were scarce or unavailable. For exam- mates from Europe and North America other countries, and only small quanti- ple, international companies working are valid for the population of Qatar. ties have been imported to Qatar: 1390 in Qatar apply their own international Little is known about occupational metric tons in 2005, decreasing to 23 standards for surveillance of occupa- exposure to carcinogens in Qatar. The metric tons in 2007 (20). Qatar has tional exposures. Information from exposure to occupational carcinogens in banned the import of chrysotile asbes- individual companies was not made different industries have been assessed in tos (21). available to us and therefore we were studies from other countries, for example Oil and gas activities represent the unable to estimate the number of work- the European CAREX [carcinogen ex- main source of revenue for the Govern- ers exposed to different occupational posure] database (11,12). The relevance ment of Qatar and include exploration, carcinogens. of such databases are likely to be limited production and refining. Technologies The levels of air pollution reported to Qatar and other EMR countries, due used for the extraction of natural gas are in Qatar exceed those reported by Eu- to the use of different materials, pro- to a large extent automated and there- ropean and North American countries, cesses and technologies. For example, fore do not need a large workforce (17). and thus may influence the country’s in Europe and North America the sand

In addition, most processes are in closed future lung cancer burden (22). PM10 used for concrete is rich in quartz, which

systems, with little potential for expo- and PM2.5 measurements from Qatar contains crystalline silica, a group 1

sure of humans to hazardous agents. substantially (23) (PM2.5 annual mean carcinogen. The frequent exposure to = 10 µg/m3) and were in the upper crystalline silica has contributed to the Lifestyle factors range of ambient air pollutants reported construction industry being classified as A 2012 survey of Qatari nationals found internationally. Particulate matter from a high-risk activity. In Qatar, the predom- that 70.1% of participants were classified outdoor air pollution is classified as inant materials used in construction are as either overweight [body mass index carcinogenic to humans by the IARC limestone and gabbro, which have lower (BMI) 25–29 kg/m2] or obese (BMI monographs programme (22). How- levels of silica compared with quartz. ≥ 30 kg/m2) and nearly half (45.0%) ever, the evidence for the association Thus, the risk of exposure to silica in the

reported a low level of physical activity. between PM10 and cancer risk is based construction industry in Qatar is likely Obesity levels were comparable in both largely on epidemiological studies from to be lower compared with Europe and sexes, with 40.0% of men and 43.0% Europe and North America (24,25). North America, with a correspondingly of women aged 18–64 years having a There are no large-scale studies that lower lung cancer risk. Qatari nationals

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are mostly employed in office-based ac- and the Marshall Islands (27). Having and North America (30). However, as tivities with low potential for exposure to a healthy body weight protects against life expectancy in Qatar increases it is known occupational carcinogens (17), cancers of the oesophagus (adeno- expected that the incidence of cancer while for the mostly expatriate workers carcinoma), colorectum, gall bladder, will increase in the future (31). Lifestyle in the construction industry, our review pancreas, breast (postmenopausal), factors are likely to play the greatest role suggests that greatest problems related endometrium, ovary, kidney (renal in cancer trends. National strategies to carcinogen exposure are likely to cell) and prostate cancer (advanced), have been developed to target obesity be environmental dust and related air while regular physical activity protects and physical inactivity in the population pollutants. against cancers of the colon, breast and and Qatar is part of the WHO Frame- A weakness of our review was lack of endometrium (7,8). A healthy body work Convention on Tobacco Control. access to information on occupational weight and regular physical activity is, Continued surveillance of different age exposures, including what agents were after tobacco control, the second most groups and evaluation of preventive used and at what levels. A further chal- important way to prevent cancer (28). measures are warranted. Relatively high lenge in assessing the cancer risk is that Given the relatively high proportion levels of ambient air pollution have been many workers in the potentially high- of overweight and obesity and that reported in Qatar, and are expected to risk occupations are non-Qatari nation- almost half of the population report contribute to the population’s future als who tend to stay in the country for a low physical activity suggests that, for lung cancer burden. There were few relatively short time (26). Cancer most Qatari nationals, lifestyle factors, in par- data on occupational exposures avail- often occurs several years after the -ex ticular obesity, physical inactivity and able to us, and therefore the influence posure; the follow-up required to assess tobacco use, could pose the greatest of carcinogens in industrial settings on cancer risk associated with occupational risk of cancer. Preventive action here is the cancer burden remains unknown. exposures may therefore be challenging likely to have the greatest influence on Future research is needed to obtain in this dynamic population. future cancer trends in Qatar. Tobacco more extensive data on the composition Data compiled by the Institute for use increases the risk of many different of environmental air pollutants and in Health Metrics and Evaluation at the cancers and therefore represents a large particular personal monitoring, as well University of Washington shows that component of the cancer risk in Qatar, occupational exposures associated with Qatar has the sixth highest prevalence although the prevalence of tobacco use new industries in the country, to fully of overweight and obesity (body-mass is comparatively low compared with understand their potential influence on index of over 25 kg/m2) among people other countries worldwide (29). the cancer burden in the population. aged 20 years and older in the world, The current cancer burden in Qatar Funding: None. after Tonga, Samoa, Kiribati, Kuwait is relatively small compared with Europe Competing interests: None declared.

References

1. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, php https://monographs.iarc.fr/ENG/Classification/Classifi- et al. GLOBOCAN 2012 v1.0. Cancer incidence and mortality cationsAlphaOrder.pdf, accessed 26 April 2016). worldwide: IARC CancerBase No. 11. Lyon, France: Interna- 7. Anderson AS, Key TJ, Norat T, Scoccianti C, Cecchini M, Ber- tional Agency for Research on Cancer; 2013. rino F, et al. European code against cancer 4th edition: obe- 2. Cancer prevention {Internet]. Geneva: World Health Organi- sity, body fatness and cancer. Cancer Epidemiol. 2015 Dec;39 zation; 2015 (Available from: http://www.who.int/cancer/ Suppl 1:S34–45. PMID:26205840 prevention/en/, accessed 26 April 2016). 8. Leitzmann M, Powers H, Anderson AS, Scoccianti C, Berrino F, 3. Deaths by cause of death, age and sex (WHO data). New Boutron-Ruault MC, et al. European code against cancer 4th York: United Nations Statistics Division; 2016 (Available from: edition: physical activity and cancer. Cancer Epidemiol. 2015 http://data un org/Data aspx?d=POP&f=tableCode%3A105, Dec;39 Suppl 1:S46-55. Epub 2015 Jul 15. accessed 26 April 2016). 9. Haj Bakri A, Al-Thani A. Qatar STEPS report 2012. Chronic 4. National cancer strategy: the path to excellence, 2011–2016. disease risk factor surveillance. Doha: Supreme Council of Doha: Supreme Council of Health; 2012 (Available from: Health; 2013 (Available from: http://www.who.int/chp/ http://nhsq info/app/media/878 , accessed 26 April 2016). steps/Qatar_2012_STEPwise_Report.pdf?ua=1, accessed 26 5. National health strategy 2011–2016. Project implementation April 2016). plans update 2013. Doha: Supreme Council of Health; 2013 10. The global adult tobacco survey fact sheet. Cairo: WHO (Available from: http://nhsq info/app/media/1029, accessed Regional Office for the Eastern Mediterranean; 2013 (Avail- 26 April 2016). able from: http://www.emro.who.int/images/stories/tfi/ 6. IARC monographs on the evaluation of carcinogenic risks to documents/FACT_SHEETS/FS_GATS_Qatar_2013.pdf?ua=1, humans. List of classifications, volumes 1–115 [Internet]. Lyon: accessed 26 April 2016). International Agency for Research on Cancer (Available from: 11. Driscoll T, Nelson DI, Steenland K, Leigh J, Concha-Barrientos http://monographs.iarc.fr/ENG/Classification/latest_classif. M, Fingerhut M, et al. The global burden of disease due to

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occupational carcinogens. Am J Ind Med. 2005 Dec;48(6):419– public_health/chrysotile_asbestos_summary.pdf, accessed 31. PMID:16299703 26 April 2016). 12. Kauppinen T, Toikkanen J, Pedersen D, Young R, Ahrens W, 22. IARC working group on the evaluation of carcinogenic risks to Boffetta P, et al. Occupational exposure to carcinogens in the humans. A review of human carcinogens. IARC Monographs European Union. Occup Environ Med. 2000 Jan;57(1):10–8. on the Evaluations of Carcinogenic Risks to Humans. Volume PMID:10711264 109. Ambient air pollution. Lyon: International Agency for Re- 13. Prevalence of noncommunicable disease risk factors in some search on Cancer; 2013. countries in Eastern Mediterranean. STEPwise survey. Geneva: 23. Air quality guidelines global update 2005. Copenhagen: WHO World Health Organization; 2013 (Available from: http:// Regional Office for Europe; 2006. www.emro.who.int/noncommunicable-diseases/informa- 24. Raaschou-Nielsen O, Andersen ZJ, Beelen R, Samoli E, Sta- tion-resources/ncd-risk-factors-prevalence.html, accessed 26 foggia M, Weinmayr G, et al. Air pollution and lung cancer April 2016). incidence in 17 European cohorts: prospective analyses from 14. Ambient (outdoor) air pollution in cities database 2014. Gene- the European Study of Cohorts for Air Pollution Effects (ES- va: World Health Organization; 2015 (Available from: http:// CAPE). Lancet Oncol. 2013 Aug;14(9):813–22. 10.1016/S1470- www.who.int/phe/health_topics/outdoorair/databases/cit- 2045(13)70279-1 PMID:23849838 ies/en/, accessed 26 April 2016). 25. Lepeule J, Laden F, Dockery D, Schwartz J. Chronic exposure 15. Engelbrecht JP, McDonald EV, Gillies JA, Jayanty RK, Casuccio to fine particles and mortality: an extended follow-up of the G, Gertler AW. Characterizing mineral dusts and other aerosols Harvard Six Cities study from 1974 to 2009. Environ Health from the Middle East–part 2: grab samples and re-suspensions. Perspect. 2012 Jul;120(7):965–70. PMID:22456598 Inhal Toxicol. 2009 Feb;21(4):327–36. PMID:19235611 26. 26. Gardner A, Pessoa S, Diop A, Al-Ghanim K, Le Trung K, 16. Engelbrecht JP, McDonald EV, Gillies JA, Jayanty RK, Casuccio Harkness L. A portrait of low-income migrants in contemporary G, Gertler AW. Characterizing mineral dusts and other aerosols Qatar. Journal of Arabian Studies. 2013;3(1):1–17. from the Middle East—part 1: ambient sampling. Inhal Toxicol. 27. Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono 2009 Feb;21(4):297–326. PMID:19235610 C, et al. Global, regional, and national prevalence of over- 17. Bulletin labor force statistics 2012. Doha: Ministry of De- weight and obesity in children and adults during 1980-2013: velopment Planning and Statistics; 2013 (Available from: a systematic analysis for the Global Burden of Disease Study http://www.qix.gov.qa/portal/page/portal/QIXPOC/Docu- 2013. Lancet. 2014 Aug 30;384(9945):766–81. PMID:24880830 ments/QIX%20Knowledge%20Base/Publication/Labor%20 28. IARC working group on the evaluation of carcinogenic risks to Force%20Researches/labor%20force%20sample%20survey/ humans. Preventive strategies. Volume 6. Weight control and Source_QSA/Labour_Force_Statistics_QSA_Bu_AE_2012.pdf, physical activity. Lyon: International Agency for Research on accessed 26 April 2016). Cancer; 2001. 18. Al-Ansary M, Iyengar S. Physiochemical characterization of 29. Asma S, Mackay J, Song S, Zhao L, Morton J, Palipundi K. The coarse aggregates in Qatar for construction industry. Interna- GATS atlas. Global adult tobacco survey. Atlanta (GA): CDC tional Journal of Sustainable Built Environment. 2013;2(1):27–40. Foundation; 2015. 19. Press F, Siever R, Grotzinger J, Jordan T. Understanding earth. 30. Cancer incidence in five continents. Volume X [Internet]. 4th ed. New York: W.H. Freeman; 2003. Lyon: International Agency for Research on Cancer [IARC 20. Virta RL. World asbestos consumption from 2003 through Scientific Publication No. 164] (Available from: http://www. 2007. Reston (VA): United States Geological Survey; 2009 iarc.fr/en/publications/pdfs-online/epi/sp164/, accessed 26 (Available from: (http://minerals.usgs.gov/minerals/pubs/ April 2016). commodity/asbestos/mis-2007-asbes.pdf, accessed 26 April 31. Salomon JA, Wang H, Freeman MK, Vos T, Flaxman AD, Lopez 2016). AD, et al. Healthy life expectancy for 187 countries, 1990–2010: 21. Chrysotile asbestos. Geneva: World Health Organization; a systematic analysis for the Global Burden Disease Study 2010. 2014 (Available from: http://www.who.int/ipcs/assessment/ Lancet. 2012 Dec 15;380(9859):2144–62. PMID:23245606

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Letter to the Editor

Medical error reporting: is it about physicians’ knowledge and their practice, or patient safety culture in the workplace?

In their original article published in the These questions are difficult to answer, current Canadian Medical Association Eastern Mediterranean Health Journal and encourage guessing, particularly for (CMA) patient safety policy framework entitled “Physicians’ knowledge and staff who have recently joined the medi- updated in 2010 (2). CMA in its policy practice towards medical error report- cal workforce or are recently appointed stated, “patient safety initiatives should ing: a cross-sectional hospital-based to the hospital. encourage and anticipate the full and study in Saudi Arabia” Alsafi et al. used Second, there were no questions appropriate disclosure to patients of a questionnaire to assess physicians’ about whether the staff were trained in relevant information that is material to knowledge and their practice in report- the area of patient safety and reporting their health and healthcare, including ing medical errors (1). However, it is medical errors, nor there were questions information about adverse events or not clear how physicians’ knowledge effects”. Also the College of Physicians on the use of technology, information related to medical error reporting, nor and Surgeons of Ontario in its recent accessibility, communication skills, pa- it is clear how the reported physician’s document (3), clearly stated the regula- tient collaboration, multi-professional practices could provide the actual rea- tions and procedures for adverse events teamwork or type of culture embedded sons for under-reporting or minimizing reporting. Furthermore, the Canadian in the hospital. the recurrence of avoidable patterns Patient Safety Institute has on its web- of higher error rates. The design of the Third, in the discussion the authors site documents on patient safety and work raises a number of issues. indicated that, “in Canada, error dis- medical error reporting recommenda- First, one would wonder about the closer is not explicitly addressed in the tion procedures (4) that the authors did validity of the questionnaire used and new Canadian Medical Association’s not refer to. how the questionnaire was constructed. Code of Ethics. In addition, most pro- One would wonder if physicians’ There are no references to show if the fessional bodies, such as the College of knowledge was the right target and how questionnaire was adopted from the Physicians and Surgeons of Ontario, such information could improve perfor- literature, nor there were justifications the Province’s regulatory body for mance. New approaches in this area aim for the questions included in the ques- physicians, have no policies requiring at building a systems approach, the de- tionnaire. Questions about “most fre- physicians to disclose errors except in velopment of a culture of patient safety quently” and “most common” medical some circumstances...”. The reference and introducing strategies to minimize errors in the hospital represented 50% of cited by the authors dated back to the recurrence of avoidable patterns of questions about physicians’ knowledge. 2001. Such statements do not reflect medical errors and poor reporting (5).

References

1. Alsafi E, Baharoon S, Ahmed A, Al-Jahdali HH, Al Zahrani S, Al College of Physicians and Surgeons of Canada; 2014 (http:// Sayyari A. Physicians’ knowledge and practice towards medi- www.royalcollege.ca/portal/page/portal/rc/common/docu- cal error reporting: a cross-sectional hospital-based study in ments/policy/culture_of_patient_safety.pdf; accessed 5 No- Saudi Arabia. East Mediterr Health J. 2015 Oct 2;21(9):655–64. vember 2015). PMID:26450862 4. Canadian Patient Safety Institute [Internet] (http://www. 2. CMA patient safety policy framework (updated 2010). Ottawa patientsafetyinstitute.ca/en/education/Pages/default.aspx, (ON): Canadian Medical Association; 2010 (https://www.cma. accessed 5 November 2015). ca/Assets/assets-library/document/en/advocacy/policy- 5. La Pietra L, Calligaris L, Molendini L, Quattrin R, Brusafer- research/CMA_Policy_CMA_Patient_Safety_Policy_Frame- ro S. Medical errors and clinical risk management: state of work_Update_2010_PD10-04-e.pdf#search=patient%20 the art. Acta Otorhinolaryngol Ital. 2005 Dec;25(6):339–46. safety, accessed 5 November 2015). PMID:16749601 3. Matlow A, Brian S. A culture of patient safety: foundation for a Royal College patient safety roadmap. Ottawa (ON): Royal

S.A. Azer Professor, Medical Education Department, King Saud University, Riyadh, Saudi Arabia ([email protected])

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Author response

To start I would like to thank you for disclosure is a key element in patient joined the hospital. We support more your interest in reading our paper “Phy- safety. Physician’s actual practices of streamlining of the questionnaire in sicians’ knowledge and practice towards medical error reporting are influenced future study to include all further ele- medical error reporting: a cross-section- by their knowledge of the existing sys- ments of missing information. al hospital-based study in Saudi Arabia” tem of disclosing medical errors. We also acknowledge the observa- and raising these legitimate questions. We acknowledge that questions and tion that the reference related to the Physicians’ knowledge of the occur- concerns raised are important to be Canadian Medical Association’s Code rence of medical errors is an important asked and addressed. Many of the pa- of Ethics should have included the up- recognition step towards better report- tient safety concepts are relatively newly dated patient safety policy framework of ing practices. If physicians underesti- embedded in the health care heritage 2010. The update includes encourage- mated the occurrence of errors, a false in Saudi Arabia. We do not expect that ment for physicians for what they refer safety environment may be created. currently the majority of our workforce as “appropriate disclosure “of adverse It is very important to distinguish is exposed to them, even less so at the events or effects. We feel that more em- between the maturity of different health time when our work was done. phasis and mandating regulations can care systems when it comes to reporting We acknowledge some of the errors. While the concepts of patient limitations of the questionnaire used, be further built in the current document. safety emerged in the United States however we feel the questions were We are very grateful for the enlight- and Europe many years ago, developing appropriate for the research aims. As ening remarks raised and we will be countries have only started to build this evident by our results, we did not have sure to bear them in mind them for our culture. Transparency in medical error many respondents who had only just future research.

Salim Baharoon, Principle investigator Department of Medicine, King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia

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WHO events addressing public health priorities

Implementing the WHO FCTC: the need to scale up tobacco control

WHO FCTC The meeting was attended by representatives of 14 The WHO Framework Convention on Tobacco Control Parties to the Convention, one country observer (Mo- (FCTC) was developed in response to the globalization of rocco) and several international experts. The participants the tobacco epidemic. It is the first international public health included representatives from ministries of health, min- treaty that provides a comprehensive approach to reduce the istries of finance and tax departments, tobacco control health and economic burden caused by tobacco. programme officers, representatives of the United Nations The WHO FCTC came into force in 2005 and, in 2008, Development Programme (UNDP) and nongovern- WHO introduced the MPOWER package of tobacco mental organizations and members of the Convention control measures, focusing on demand reduction, to help Secretariat (CSF). countries implement the WHO FCTC. MPOWER focuses Challenges and ways forward on six key tobacco control measures, each corresponding to at least one provision of the treaty: Monitor tobacco use and With regard to taxation, there are major gaps in the countries prevention policies; Protect people from tobacco use; Offer of the Region. Many countries implement customs fees help to quit tobacco use; Warn about the dangers of tobacco rather than excise taxes and many have a very low rate of taxes. use; Enforce bans on tobacco advertising, promotion and Even in some countries where the taxation levels are high and sponsorship; Raise taxes on tobacco. up to the maximum recommended levels, the prices are still In the Eastern Mediterranean Region (EMR), 19 of the low and products are still very affordable. 22 member countries are party to the WHO FCTC and they The main factor in controlling illicit tobacco trade is have made some progress through legislations based on the governance, not pricing. Evidence shows that smuggling is Convention, including total bans on tobacco advertising, not linked to taxation levels but rather to poor governance smoking bans in indoor public places, pictorial health warn- and weak enforcement in areas such as customs. Contrary ings on tobacco packaging and increased tax on tobacco to tobacco industry claims, increased smuggling does not products. automatically follow tax increases. Tobacco taxation is a cost- The WHO Regional Office for the Eastern Mediter- effective tobacco control policy and benefits governments ranean organizes an annual intercountry meeting to monitor from both an economic and health standpoint. The tobacco progress on the implementation of the WHO FCTC in industry is making concerted efforts to stop the increase in the Region, identify challenges and propose ways forward. tobacco prices and taxes, and to make it difficult for countries The 2015 meeting was held on 26–28 October 2015 in to revisit their taxation systems and policies. Cairo, Egypt and focused on two core areas: 1) the general There is a need for a balanced approach in implementing implementation of the WHO FCTC with its demand and the demand and supply side measures. Countries should supply side measures; and 2) the implementation of Article aim at implementing the highest level measures of all poli- 6 of the WHO FCTC, adopted by the Conference of Parties cies rather than introducing softer measures in different (COP) in October 2014, with its taxation increase and price policies. measures. Implementation, ratification and entry into force of the Specific objectives included: strengthening Parties’ imple- Protocol to Eliminate Illicit Trade in Tobacco Products are mentation of the WHO FCTC and policies related to water a priority for the Region. Countries need to expedite the pipe tobacco and tobacco industry interference; promoting process at the national level with the support of the WHO ratification/accession to the Protocol to Eliminate Illicit Trade FCTC Secretariat and the WHO Regional Office. Key in Tobacco Products by the Parties; analysing the regional sta- element in speeding up the process at the national level in tus for taxes on tobacco products; identifying the way forward include multisectorality and protecting the process from the for improving implementation of the WHO FCTC, including vested interests of the tobacco industry (in some countries the adoption of new taxation policies in Member States. where there are national monopolies the tobacco industry is

This article is abridged from the on the Annual Intercountry Meeting on the Implementation of the WHO Framework Convention on Tobacco Control (http://applications.emro.who.int/docs/IC_Meet_Rep_2015_EN_16717.pdf?ua=1)

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Box 1 Actions to scale up tobacco control in the Region

WHO FCTC Article 6 Countries 1. Advance the issue of tobacco tax increases, in line with WHO FCTC Article 6. With the Regional Director’s letter, forward the proposals on tobacco taxation developed during the meeting to Ministers of Health as well as Ministers of Finance. 2. Start national analyses related to taxation status in order to identify gaps, priorities and ways forward. WHO and CSF 3. Raise taxation issues with regional bodies such as the League of Arab States, the Organization of Islamic Confer- ence and the Gulf Cooperation Council through direct communications and letters from the Regional Director and head of the CSF. 4. Provide tailored technical support to Parties based on parties’ official requests to WHO and CSF.

WHO FCTC general implementation Countries 5. Scale up political commitments: participants attending the meeting should to continue to engage their political decision-makers at all levels through regular updates and technical briefings. 6. Encourage regulation of all tobacco products, including water pipes and e-cigarettes. 7. Strengthen implementation of smoke-free policies and implement appropriate awareness raising programmes to promote such measures. 8. Address tobacco advertising, promotion and sponsorship (TAPS) comprehensively to protect against the vested interests of the tobacco industry. 9. Finalize a proposal for the Seventh session of the Conference of the Parties (COP7) for discussion on TAPS in movies/drama/TV. 10. Re-examine the status of Article 11 implementation and safeguard pictorial health warnings from the tobacco industry interests. 11. Take all necessary steps to ratify/accede to the Protocol to Eliminate Illicit Trade in Tobacco Products as soon as possible to accelerate its entry into force.1 WHO and CSF 12. Appoint an informal volunteer focal point from countries of the Region for each annual WHO FCTC meeting to follow up with countries as well as WHO and CSF on the status of the recommendations. 13. Develop copyright-free warnings for Parties. 14. Consider conducting regional research on illicit trade in the Region. 15. Provide the technical assistance needed to support the process of ratification/accession to the Protocol.

1 Since the meeting, Iraq and Saudi Arabia have become Party to the Protocol.

involved in the decision-making process related to the proto- Needed actions col ratification/accession). In light of these challenges, a number of actions for the coun- Tobacco advertising, promotion and sponsorship tries, and WHO and CSF were identified in order to advance (TAPS) in movies/drama/TV is undermining other to- implementation of the WHO FCTC and effectively scale up bacco control activities in the Region and COP guidance is tobacco control in the Region. Box 1 shows some of the main needed on how to control tobacco use in these media. recommended actions.

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Book 22-03.indb 231 6/14/2016 9:00:11 AM Members of the WHO Regional Committee for the Eastern Mediterranean املجلة الصحية لرشق املتوسط Afghanistan . Bahrain . Djibouti . Egypt . Islamic Republic of Iran . Iraq . Jordan . Kuwait . Lebanon هى املجلة الرسمية التى تصدر عن املكتب اإلقليمى لرشق املتوسط بمنظمة الصحة العاملية. وهى منرب لتقديم السياسات Libya . Morocco . Oman . Pakistan . Palestine . Qatar . Saudi Arabia . Somalia . Sudan . Syrian Arab واملبادرات اجلديدة ىف اخلدمات الصحية والرتويج هلا، ولتبادل اآلراء واملفاهيم واملعطيات الوبائية ونتائج األبحاث وغري Republic . Tunisia . United Arab Emirates . Yemen ذلك من املعلومات، وخاصة ما يتعلق منها بإقليم رشق 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.

EASTERN MEDITERRANEAN HEALTH JOURNAL البلدان أعضاء اللجنة اإلقليمية ملنظمة الصحة العاملية لرشق املتوسط IS the official health journal published by the Eastern Mediterranean Regional Office of the World Health Organization. It is a forum for the presentation and promotion of new policies and initiatives in health services; and for the exchange of ideas, con‑ األردن . أفغانستان . اإلمارات العربية املتحدة . باكستان . البحرين . تونس . ليبيا . مجهورية إيران اإلسالمية .cepts, epidemiological data, research findings and other information, with special reference to the Eastern Mediterranean Region اجلمهورية العربية السورية . اليمن . جيبويت . السودان . الصومال . العراق . عُ ام ن . فلسطني . قطر . الكويت . لبنان . مرص ‑It addresses all members of the health profession, medical and other health educational institutes, interested NGOs, WHO Col laborating Centres and individuals within and outside the Region. املغرب . اململكة العربية السعودية LA REVUE DE SANTÉ DE LA MÉDITERRANÉE ORIENTALE EST une revue de santé officielle publiée par le Bureau régional de l’Organisation mondiale de la Santé pour la Méditerranée orientale. Elle offre une tribune pour la présentation et la promotion de nouvelles politiques et initiatives dans le domaine des ser‑vices de santé ainsi qu’à l’échange d’idées, de concepts, de données épidémiologiques, de résultats de recherches et d’autres Membres du Comité régional de l’OMS pour la Méditerranée orientale 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 collabora‑ Afghanistan . Arabie saoudite . Bahreïn . Djibouti . Égypte . Émirats arabes unis . République islamique d’Iran teurs de l’OMS et personnes concernés au sein et hors de la Région. Iraq . Libye . Jordanie . Koweït . Liban . Maroc . Oman . Pakistan . Palestine . Qatar . République arabe syrienne Somalie . Soudan . Tunisie . Yémen

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/

EMHJ is abstracted/indexed in the Index Medicus and MEDLINE (Medical Literature Analysis and Retrieval Systems on Line), ISI Web of knowledge, the Cumulative Index to Nursing and Allied Health Literature (CINAHL), Embase, Lexis Nexis, Scopus and the Index Medicus for the WHO Eastern Mediterranean Region (IMEMR). Correspondence

Editor-in-chief Eastern Mediterranean Health Journal ©World Health Organization 2016 WHO Regional Office for the Eastern Mediterranean All rights reserved P.O. Box 7608 Nasr City, Cairo 11371 Disclaimer Egypt The designations employed and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of the World Health Organization concerning the legal status of any country, territory, city or area or of Tel: (+202) 2276 5000 its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted lines on maps represent approximate border Fax: (+202) 2670 2492/(+202) 2670 2494 lines for which there may not yet be full agreement. The mention of specific companies or of certain manufacturers’ products Email: [email protected] does not imply that they are endorsed or recommended by the World Health Organization in preference to others of a similar nature that are not mentioned. All reasonable precautions have been taken by the World Health Organization to verify the information contained in this publication. However, the published material is being distributed without warranty of any kind, either express or implied. The responsibility for the interpretation and use of the material lies with the reader. In no event shall the World Health Organization be liable for damages arising from its use. The named authors alone are responsible for the views expressed in this publication. Subscriptions and Permissions Publications of the World Health Organization can be obtained from Knowledge Sharing and Production, World Health Organization, Regional Office for the Eastern Mediterranean, ISSN 1020-3397 PO Box 7608, Nasr City, Cairo 11371, Egypt (tel: +202 2670 2535, fax: +202 2670 2492; email: [email protected]). Requests for permission to reproduce, in part or in whole, or to translate publications of WHO Regional Office for the Eastern Mediterranean – whether for Cover designed by Diana Tawadros sale or for noncommercial distribution – should be addressed to WHO Regional Office for Internal layout designed by Emad Marji and Diana Tawadros the Eastern Mediterranean, at the above address; email: [email protected]. Printed by WHO Regional Office for the Eastern Mediterranean Cover photograph ©World Health Organization

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Editorial

Moving away from the comfort zone of tobacco control policies to the highest level of implementation...... 161 Research articles

Risk factors for neonatal intensive care unit admission in Amman, Jordan...... 163 Trend of bacterial meningitis in Bahrain from 1990 to 2013 and effect of introduction of new vaccines...... 175 Change in attitudes and knowledge of problem drug use and harm reduction among a Eastern Mediterranean community cohort in Kabul, Afghanistan...... 183 Accuracy of the VITEK® 2 system for a rapid and direct identification and susceptibility testing Health Journal of Gram-negative rods and Gram-positive cocci in blood samples...... 193 Review Routine immunization services in Pakistan: seeing beyond the numbers...... 201 La Revue de Santé de Volume 22 Number 3 Short communications la Méditerranée orientale Responding to physical and psychological health impacts of disasters: case study of the Iranian disaster rehabilitation plan...... 212 Environmental carcinogen exposure and lifestyle factors affecting cancer risk in Qatar:

findings from a qualitative review...... 219 March 2016 Letter to the Editor

Medical error reporting: is it about physicians’ knowledge and their practice, or patient safety culture in the workplace?...... 228

WHO events addressing public health priorities

Implementing the WHO FCTC: the need to scale up tobacco control...... 230

Effective and affordable tobacco control policies and measures are well established, including banning smoking in all public places and taxing tobacco products. Countries of the Region need to step up their implementation of tobacco control measures in order to make greater progress towards achieving the targeted 30% reduction in tobacco use by 2025.

املجلد الثاين والعرشون / عدد Volume 22 / No. 3 3 مارس/آذار March/Mars 2016

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