Emerging and Re-emerging Infectious Diseases in the WHO Eastern Mediterranean Region, 2001-2018

Introduction

Emerging infectious diseases (EIDs) are those that have recently appeared within a population or those whose incidence or geographic range is rapidly increasing or threatens to increase shortly. Re-emerging infectious diseases (RIDs) are those which were previously controlled, but have again risen to be a significant health threat.^1,2 The emergence of high-threat pathogenic diseases has increased in recent years globally.² Almost 75% of recently emerged diseases afflicting humans have a zoonotic origin.²

Many countries in the World Health Organization (WHO) Eastern Mediterranean Region (EMR) are affected directly or indirectly by acute and protracted humanitarian emergencies, which have led to an unusually high number of internally displaced people and refugees living in overcrowded, overburdened camps, with little or no access to basic social and healthcare services.³ Many factors are contributing to the emergence or re-emergence of high-threat pathogenic diseases including pathogen’s adaptation or resistance, host behavior such as migration, international travel, human-animal interaction, poverty, climate change, and industrial and economic development.⁴

WHO EMR includes countries from North Africa to southwest Asia, with a total population of 670 million, Pakistan, Egypt, and Iran with about 200, 105, and 85 million people are respectively the most populated countries in this region.⁵

EIDs and RIDs occur as a result of interconnection among social, economic, biological, technological, and ecological factors. A high percentage of EMR populations live in poverty with the regional average gross domestic product per capita lagging behind the global average,⁶ with significance in Somalia, Afghanistan, Yemen, Syria, and Sudan⁷; thus, further predisposing the region to EIDs and RIDs. Different climate and living conditions lead to the spread of various diseases,⁸ with ecological changes playing an important role in the re-emergence of infectious diseases.⁹ The periodic mass gathering of pilgrims in the EMR, namely to Saudi Arabia and Iraq, can also be a threat for outbreaks of EIDs and RIDs.¹⁰ Increased conflict and political instability in the region that lead to large population movement are other major causes of elevating the risk of spreading various diseases (eg, diphtheria, cholera, and leishmaniasis).¹¹

Recent outbreaks of EIDs and RIDs in the EMR include Crimean Congo hemorrhagic fever (CCHF) in Afghanistan¹², chikungunya in Pakistan and Sudan,^13,14 cholera in Somalia, and Yemen,¹⁵ diphtheria in Pakistan and Yemen,^16,17 influenza H5N1 in Egypt,¹⁸ leishmaniasis in Pakistan, Syria and Afghanistan,^19-21 measles in Pakistan and Afghanistan,^16,22 Middle East respiratory syndrome (MERS) in Arabian Peninsula,^23-25 plague in Afghanistan,²⁶ polio in Afghanistan and Pakistan,^27,28 and Q fever in Afghanistan and Iraq.^29,30 The magnitude of many of EIDs and RIDs has not been currently verified in some EMR countries. The first step in forecasting, preparing, and control of these diseases is to ascertain its existence and frequency. This paper aims to review the epidemiological situation of the EIDs and RIDs in the EMR between 2001 and 2018.

Methods

This paper is a narrative review. An exhaustive list of emerging and RIDs was identified through a literature search. The preliminary list was then shared with EMR 17 experts using Delphi method. The experts covered a range of specialities, including microbiology, epidemiology, and clinical infectious disease. Based on the expert’s opinion, a final list of infectious diseases of global concern in EMR was identified and approved.

A review about the epidemiological situation of the EIDs and RIDs in the EMR was conducted. A complete list of studies in the field was prepared following a systematic search approach. Studies that were purposively reviewed were identified to summarize the epidemiological situation of each targeted infectious disease in different EMR countries. Accessible electronic and hand-search of grey literature across all countries of the region were searched.

Systematic Search of Literature

Electronic databases were carefully searched using Medical Subject Headings terms and keywords, by the name of each of the targeted diseases or their causative agent and the name of each country in the region to extract the diseases reported between 2001 and 2018. The extensive databases included: Google Scholar, Midline, Web of Science, ScienceDirect, Scopus, Medline. We also searched grey literature via a general internet search, Web of Science, Weekly Epidemiological Monitor, WHO/EMRO, situation updates, annual reports, and report publications by the WHO, the official WHO website, and ProMED. The reference lists of all relevant articles were hand-searched to identify further any additional studies that may not have been captured by extensive searches.

Screening of Potentially Relevant Citation

Two investigators assessed titles and abstracts for relevance to the key questions using prespecified inclusion and exclusion criteria. Full-text articles identified by either investigator as potentially relevant were retrieved for further review and examined by two investigators independently.

All outcomes were adequately covered in the EndNote^® reference management software (version X5, Thomson Reuters, Philadelphia, PA, USA).

Inclusion Criteria

Eligible subjects invariably had to satisfy the following inclusion criteria sufficiently including, study designs: Published papers from 2001 and 2018 that reported the epidemiological situation of the targeted diseases in the region were included. The ultimate goal was to typically identify related systematic reviews, review articles, case reports and original articles and it was limited to Arabic and English language publications.

Quality Assessment

A narrative review was based on high-quality evidence. The methodological quality of studies that were a candidate for data extraction for this narrative review was subjectively appraised by two investigators, considering the following criteria: (a) No evidence of selection bias, (b) Proper sample size, and (c) Negligible publication bias (for systematic reviews).

Disagreements were resolved between the two investigators by discussion. A flowchart of the study selection process is illustrated in Figure 1.

Close

Figure 1. A Flow Chart Depicts the Stages of Retrieving References, Checking Eligibility Criteria, and Including the Final Articles Into The Review.

Data Abstraction and Analysis

Extracted data were abstracted into a customized Excel spreadsheet, extensive database by one investigator and verified by a second investigator. All related papers found were carefully reviewed and succinctly summarized for potential inclusion in this report. The included diseases are listed in three groups (viral, bacterial, and parasitic EIDs and RIDs) alphabetically by common name.

Results

Viral Emerging and Re-emerging Infectious Diseases

Acute hepatitis A and E: Except for a few published articles and outbreak reports, very limited data are available about the prevalence of hepatitis A virus (HAV) and hepatitis E virus (HEV) from countries in the EMR.³¹ HAV and HEV are reported in high frequency in some studies in Tunisia (84%),³² Yemen (86%),³³ Iran (86%), Iraq (96%),³⁴ Egypt (100%),³⁵ and Libya (100%).³⁶ Morocco is an intermediate endemic area for the HAV infection.³⁷ Most rural areas have high anti-HAV antibody prevalence due to consumption of sewage-contaminated water and use of indoor dry pits.³⁸ Several outbreaks of HAV infection have erupted among tourists from European countries.³⁹ There were major HAV outbreaks in Syria and Lebanon in 2013 and 2014, concurrent with the Syrian crisis and influx of refugees.^40,41

In Iran, the frequency of HEV varied from 2.3% to over 40%,⁴² and have reported 20% in United Arab Emirates (UAE) in mothers,⁴³ 19.4% in Iraq in blood donors,³⁴ 13% in Egypt in workers,⁴⁴ 10% in Yemen,³³ 3% in Pakistan,⁴⁵ and 0.3% in Saudi Arabia.⁴⁶ According to reports from Pakistan, HAV and HEV are responsible for more than 19% and 12% of all newly diagnosed cases of viral hepatitis, respectively.³¹

Alkhurma hemorrhagic fever (AHF): AHF is a zoonotic viral disease that emerged in 1995 in Saudi Arabia.⁴⁷ In the initial stages of the disease discovery, high mortality rates of up to 25% were reported.⁴⁸ As the disease became better known and recognizable, identification of subclinical infections lowered the mortality rates to about 1.3%.⁴⁹ There is still a knowledge gap regarding the transmission pathways of the disease.⁵⁰

AHF has been reported from Saudi Arabia and Egypt.^51,52 Seropositive cases and AHF virus-infected Amblyomma lepidum ticks have been reported in Djibouti.⁵³

Avian influenza (H5N1): The virus was reported in 16 countries and is expected to expand its range further. In 2006, H5N1 spread rapidly through the EMR with large non-human (mostly avian) outbreaks in Afghanistan, Djibouti, Egypt, Iran, Iraq, Jordan, occupied Palestinian territories, Pakistan, and Sudan. Since then the H5N1 has become endemic in Egyptian poultry.⁵⁴ The circulation of the virus was confirmed in Saudi Arabia, Egypt, and Libya.^55,56 Since 2006, Human cases of H5N1 were reported only from Egypt, Iraq, Djibouti, and Pakistan.⁵⁷ However, Egypt has been the most affected country in the region where the disease has remained endemic, with frequent epizootic cases in addition to 356 reported human cases, including 121 deaths since October 2016, the highest number of H5N1 human cases (42%, 356/854) in the world.^58,59 A recent analysis demonstrated that the most important environmental predictors for the spread of the disease in the Middle East are the environmental temperature during the warmest quarter in correlation with high transmission rates within the livestock system with Egypt, Kuwait, Saudi Arabia, and Sudan.⁶⁰ While nearly all cases in EMR have been associated with contact with infected birds, human-to-human transmission of H5N1 has also been indicated in Djibouti, Iraq, and Pakistan, but limited.⁶¹

Chikungunya: Outbreaks of Chikungunya have only been documented in Djibouti, Pakistan, Saudi Arabia, Somalia, Sudan, and Yemen. Imported cases are also reported from Oman.^14,62 Nevertheless, serological studies in other countries such as Egypt, Iraq, Iran, and Kuwait, have reported seropositivity cases.⁶³ The earliest description of the disease in the EMR goes back to 1658 in Egypt. However, the disease presence was confirmed in 2011 in Yemen after a major outbreak with over 15 000 suspected cases.⁶⁴

Similarly, in Pakistan, the serological evidence of disease was first identified in 1983, but no further cases had been identified until 2011. Since then, the total number of infected cases drastically increased to 8330 reported cases in 2017 compared to 405 cases found in the previous year.^65,66 Considering the presence of the competent vectors and international travel of viremic patients between Eastern Mediterranean countries, there seems to be a hidden crisis with a high possibility of transmission and spread of the disease into neighboring chikungunya virus-free countries.⁶³

CCHF: So far, human cases of CCHF have been reported from 10 out of 22 countries in EM region including Afghanistan, Iran, Iraq, Oman, Pakistan, Palestine, Saudi Arabia, Sudan, Tunisia, and UAE.^67-70 Iran, Pakistan, and Afghanistan are countries reporting 50 or more CCHF cases per year.^71-73 The CCHF virus genome has been identified in ticksin Morocco and Syria.^74,75 Moreover, serological studies of livestock have identified the disease in Egypt and Somalia.⁶⁷ In Oman, from 2011-2017, the CCHF patients has steadily increased, the highest cases were reported in 2015.⁷⁶

Dengue: There is limited information about the situation of the disease in EMR. Outbreaks of dengue have occurred in Djibouti, Oman, Pakistan, Saudi Arabia, Somalia, Sudan, Yemen, and Egypt.^77-79 Additionally, serological investigations have shown seroprevalence of dengue in Afghanistan, Iran, Kuwait, Lebanon, Qatar, and Syria.⁸⁰ The main mosquito vectors for dengue virus, Aedes aegypti and Aedes albopictus, have been reported from 15 countries in the region including Afghanistan, Djibouti, Egypt, Iran, Jordan, Lebanon, Oman, Pakistan, Palestine, Saudi Arabia, Somalia, Sudan, Syria, Tunisia, and Yemen.^81-84 However, little is known about the presence of infected vectors in other EM countries, due to the inadequate entomological surveillance systems in most of these countries. In 2017, Pakistan, Egypt, and Sudan reported 125 316, 245, and 139 dengue cases, respectively.⁶⁶

A total of 6777 suspected dengue cases were reported in 2015 in Yemen after the civil war, which began in 2015, causing widespread destruction of the infrastructure and therefore enabling dengue to become endemic in this country.⁸⁵

Measles: In 1997, all EMR countries adopted a resolution to eliminate measles by 2010. This effort resulted in a 93% reduction in mortality from measles between 2000 and 2008. Despite significant progress, the goal was not reached by 2010, and the date was revised to 2015 and then again to 2020.⁸⁶ Unlike the predictions, the total number of measles cases increased from over 12 000 cases in 2008 to over 36 000 in 2012.⁸⁷ Between 2013 and 2018, 144 966 cases of Measles were reported in the region.⁸⁸ All countries in the region have moved to case-based measles surveillance with laboratory confirmation implementing nationwide surveillance and two countries (Somalia and Sudan) implementing sentinel surveillance. Countries affected by war, such as Syria, Yemen, Iraq, Afghanistan, and Lebanon reported high numbers of measles cases, for example during 2013-2016, 7000 cases of measles were reported in Syria, and 5773 cases were reported from Yemen during 2012-2017.^89-91 Pakistan also reported a high number of measles patients due to low vaccination coverage.⁹² Djibouti, Somalia, and Sudan are also countries in the region with high incidence.⁸⁷ Bahrain, Egypt, Iran, Jordan, Morocco, Palestine, and Tunisia have progressed drastically and reported a very low incidence of endemic measles.⁹³ Nevertheless, the surge of disease in countries affected by armed conflicts and political instability shows how easily it can return, especially with the low immunization coverage.

MERS: MERS was first reported in Saudi Arabia in 2012.⁹⁴ In EMR, 12 countries (Bahrain, Egypt, Iran, Jordan, Kuwait, Lebanon, Oman, Qatar, Saudi Arabia, Tunisia, UAE, and Yemen) have reported cases of MERS.^95-98 By the end of 2018, a total of 2279 confirmed cases were reported globally with the majority of cases in Saudi Arabia (1901 laboratory-confirmed cases, including 732 related deaths with a case–fatality ratio of 38.5%).⁹⁹ Most of the primary MERS cases outside Arabian Peninsula were linked with either by travel or residence in the countries of Arabian Peninsula.¹⁰⁰ Transboundary movement of humans and camels among the Arab countries could be a source of MERS coronavirus (MERS-CoV) transmission.¹⁰¹ Clusters of MERS secondary cases were reported either in hospital or family settings in Saudi Arabia, UAE, and Iran.^102-104 In Saudi Arabia, hospital outbreaks in 2015-2018 resulted in 334 cases and 102 associated deaths, and approximately 30% of these reported cases were healthcare workers.¹⁰⁵ In Qatar, MERS pattern were mostly sporadic within the primary cases. It may be due to Qatar One Health approach to challenge MERS-CoV, and infection protection and control system in healthcare settings.¹⁰⁶

Egypt, Qatar, UAE, Oman, Morocco, and Sudan, among other countries within the EM region carried out surveillance studies on dromedary camels. Results obtained revealed high seropositivity in Egypt (84.5%) and Qatar (59% and 79%); besides, MERS-CoV genetic material was identified in 6.57%, 3.8%, and 1.6% of sampled camels from Oman, Egypt and UAE, respectively.^25,107-112

Rabies: Currently, zoonotic rabies remains mostly in dogs as the principal reservoir in the Middle East.¹¹³ Incidence from foxes was reported in UAE and Oman, and from wolves in Syria.¹¹⁴ Rabies is reported endemic in Egypt, Iran, Iraq, Pakistan, Sudan, Tunisia, Morocco, Syria, Yemen, Jordan, Oman, Palestine, Lebanon, and Saudi Arabia.^115,116 The UAE, Bahrain, and Kuwait are the only countries in the region that are considered rabies-free.¹¹⁵ Libya, Somalia, and Djibouti have no information available about rabies in humans or animals.¹¹⁶ The disease rate in animals has sharply increased in Lebanon from 2010-2016 coinciding with the beginning of Syrian conflict.¹¹⁷

Rift Valley fever (RVF): Outbreaks of RVF have been documented in the Arabian Peninsula in Yemen and Saudi Arabia (2000, 516 cases with 87 deaths),^118-120 Egypt (2003, 148 cases with 27 deaths), Somalia (2006-2007, 114 cases with 51 deaths) and Sudan (2007-2008, 738 cases with 230 deaths).^121,122 In 2017, seropositive livestock was reported in western Iran.¹²³ With the virus showing high competence for a wide range of mosquitoes, the WHO predicts future outbreaks in Egypt, Sudan, Morocco, Saudi Arabia, and Yemen.¹²⁴

Sandfly fever: Although research has demonstrated the circulation of sandfly virus in Afghanistan, Egypt, Iran, Iraq, Morocco, Pakistan, Palestine, Tunisia, Saudi Arabia, Somalia, and Sudan,^125-127 little is known about the epidemiology of sandfly fever in the EMR. Dashli virus belonging to the Sicilian serogroup and two cases of severe encephalitis caused by sandfly fever virus were reported from Iran and occupied Palestine.^128-130 Furthermore, antibodies against sandfly fever virus have been detected in Iran.¹³¹ In 2010-2011, a serological investigation in Djibouti indicated the circulation of Toscana-related viruses.¹³² In 2007, an outbreak of sandfly fever was reported from Lebanon with 700 cases.¹³³ In 2017, cases were also reported from Afghanistan.¹²⁵

West Nile fever (WNF): Human seropositive cases of WNF have been reported in Afghanistan, Djibouti, Egypt, Iran, Iraq, Jordan, Lebanon, Libya, Morocco, Pakistan, Sudan, Tunisia, and Yemen.¹³⁴ WNF infection in Culex mosquitoes was demonstrated in Djibouti, Egypt, Iran, and Tunisia.¹³⁴ This indicates the widespread circulation of WNF virus in the EMR and underlines the requirement for integrated surveillance programs. In 2018, an outbreak of WNF with 377 suspected cases, out of which 49 cases were laboratory-confirmed, was reported from Tunisia.¹³⁵

Poliomyelitis: In April 2013, a case of wild poliovirus was detected in Somalia, which quickly spread, affecting 194 people by the end of 2013. The long-term political instability in Iraq and Syria means they are key at-risk countries for re-emergence of polio.¹³⁶ Syria had a disease outbreak in 2014 that was closely associated with the virus originating from Pakistan. In 2017, Syria was affected by circulating vaccine-derived poliovirus.¹³⁷ The last reported polio cases in Somalia were five new cases in 2014.¹³⁸ In 2017, 22 cases of wild poliovirus were found in Afghanistan and Pakistan, of which increased to 33 cases in 2018.^28,66 Today the disease is only seen in Afghanistan, Pakistan, and Nigeria where vaccination was not fully covered.¹³⁹ As the virus remains present in the EMR, all countries in the region are still at high risk for re-emergence of the disease.

Bacterial Emerging and Re-emerging Infectious Diseases

Cholera: Cholera is a disease resulting from poor sanitation and living conditions. The disease is widespread across the EMR. Between 2010 and 2016, Iran, Afghanistan, Pakistan, Yemen, Iraq, and Somalia reported the disease.^140-142 In 2017, the largest outbreak of cholera in regional history was witnessed in Yemen with 1.3 million cases, and over 2500 deaths were reported by the end of 2018.¹⁴³ The second most affected country in the EMR is Somalia reporting 75 414 cases and 1007 associated deaths since the outbreak started in 2017. Other countries in the region that reported imported cases of cholera in 2017 were Qatar (5), Saudi Arabia (5), UAE (12), and Iran (625).¹⁴⁴ There are concerns about the rise of antibiotic resistance against cholera, due to mobile genetic elements in Yemen.¹⁴⁵

Diphtheria: Pakistan (930 cases), Iran (631 cases), and Sudan (225 cases) are among the list of countries with the highest prevalence of diphtheria between 2010 and 2017.^146,147 Between 2001 and 2018, cases of diphtheria are also reported to the WHO from Afghanistan, Iraq, Lebanon, Qatar, Saudi Arabia, Somalia, and Yemen,¹⁷ and no cases of diphtheria were reported from Bahrain, Djibouti, Egypt, UAE, Jordan, Kuwait, Morocco, Oman, and Tunisia.¹⁴⁷ Furthermore, countries such as Libya and Syria, which have been involved in civil wars, have not been evaluated for disease presence. In Yemen, due to ongoing war resulting in disruption of the healthcare system and lower vaccination coverage, a total of 2609 cases of the disease were reported by the end of 2018,¹⁷ even though the last outbreak in Yemen was in 1982. These outbreaks represent the great potential of diphtheria to re-emerge in disease-free areas and become endemic.¹⁴⁶

Meningococcal meningitis: The majority of the cases of meningococcal meningitis occur in sub-Saharan African countries. In EMR, Sudan is the only country at high risk of the disease; however, other countries, mainly North African countries, are also at risk.¹⁴⁸ Sudan has received a high burden of disease, experiencing several large outbreaks in 2013.^148,149 In 2016, the meningitis A vaccination was introduced into Sudan’s routine immunization program.¹⁵⁰ In 2017, an outbreak of meningitis was reported in Yemen with 2982 cases and 37 deaths.⁶⁶

Although meningococcal meningitis remains an important cause of endemic and epidemic disease across the region, published epidemiological data is fragmented and limited, and the use of vaccines has helped minimize the prevalence of meningococcal meningitis.^151,152 The meningitis belt is highly connected by Muslim pilgrims taking part in the annual Hajj ceremony, gathering in Saudi Arabia, as the congestion of people promotes increased carrier rates of meningitis.¹⁴⁸ The Global Meningococcal Initiative has recommended that EMR countries should mandate vaccination; especially those in which the Hajj is obligatory.

Plague: An outbreak of plague was reported in Afghanistan in 2007, and 17 out of 83 presumed cases became fatal.²⁶ In 2009, 3 cases of plague were reported from Libya after 25 years of disease absence.¹⁵³ Two outbreaks occurred in the years 2009 and 2011 in a coastal town in Libya.^154,155 Western Iran has remained as endemic areas for the plague. A study in 2011 in this region detected Yersinia pestis in 1.02% of trapped rodents and 3.42% of dogs.¹⁵⁶ The circulation of plague among domestic and wild animals in the region indicates possible re-emergence of human plague outbreaks.¹⁵⁷

Q Fever: All countries in the region have detected the disease in humans except Bahrain, Djibouti, Palestine, and UAE.^30,158-163 There was an outbreak of the disease among US military soldiers in Western Iraq in 2005.²⁹ A similar outbreak was reported among British soldiers in Afghanistan in 2008.¹⁶⁰ A systematic review reported 19% of Q fever seroprevalence in North Africa.¹⁶²

Tularemia: Most of the EMR countries have not reported the disease in recent years due to lack of laboratory facilities and healthcare workers’ suboptimal awareness of the disease.^164,165 Iran is the only country in the region, reporting the disease and contaminated water is the main source of infection.^164,166 However, studies on rodents and hares in Iran,¹⁶⁷ on ticks in Yemen,¹⁶⁸ and ticks and abattoir workers in Egypt found samples positive for Francisella tularensis.¹⁶⁹

Parasitic Emerging and Re-emerging Infectious Diseases

Leishmaniasis: All EM countries are reporting the cutaneous and mucocutaneous forms, though the visceral form has limited reports in this region.¹⁷⁰ Six of the ten countries with the highest reported cutaneous leishmaniasis in the world are located in the EMR including Syria, Afghanistan, Iraq, Iran and Pakistan, and Tunisia.¹⁷¹ The incidence of leishmaniasis has generally decreased in EMR; however, this region still accounts for 70% of all leishmaniasis cases across the world.¹⁷² The zoonotic form of visceral leishmaniasis is endemic in Iran.¹⁷³ In Iraq, most leishmaniasis cases are wet type cutaneous form.¹⁷⁴ Studies in Yemen have found Leishmania tropicaas the main causative agent of leishmaniasis.¹⁷⁵Leishmania tropicais more prevalent in Morocco with a rate of 30%-40% in several districts.¹⁷⁶ In 2016 and 2017, outbreaks of leishmaniasis were reported in Pakistan.¹⁷⁷ In 2017 in a study in Saudi Arabia, 8.3% of studied individuals were positive for cutaneous leishmaniasis.¹⁷⁸

In recent years, the incidence of cutaneous leishmaniasis has increased in Syria.^179,180 Lebanon, Iraq, and Egypt are affected due to Syrian refugee migration. Leishmania tropicais detected in 85% of the Syrian refugee patients in Lebanon.¹¹ Eastern Libya, similar to Syria and Yemen, has reported the outbreaks of cutaneous leishmaniasis.^181,182

Discussion

EMR is a hotspot for EIDs and RIDs. Although it’s difficult to compare the extend and burden of EID and RIDs in this region with other regions, the number of outbreaks caused by emerging and re-emerging infectious pathogens has increased in the past two decades in this region, greatly affecting social and economic development. The region is especially susceptible to outbreaks of these high-threat pathogens due to the presence of various humanitarian emergencies, fragile health systems, internal conflicts, lack of accurate data, fragile ecosystems, and increased population movement. In recent years, the frequency, duration, and scale of disease outbreaks have escalated for most of these diseases. Many disease outbreaks have been detected and managed in the region such as MERS in the Arabian Peninsula, cholera in Iraq, Somalia and Yemen, Avian influenza A (H5N1) in Egypt, CCHF in Afghanistan, Iran and Pakistan, and dengue fever in Yemen, Sudan and Pakistan (Figure 2, and Table 1). There is a need for a better understanding of disease transmission, preparedness for disease emergence, detection of pathogens and vectors, and implementation of high-impact control and interventions for prevention. This is especially difficult considering the weak surveillance systems of many countries due to limited diagnostic capacities and human resources. Extensive training programs on disease surveillance and response to health emergencies are needed now more than ever in this region.

Close

Figure 2. EIDs in Humans Reported in the EMR, 2001-2018. Abbreviations: EMR, Eastern Mediterranean Region; EIDs, emerging infectious diseases. Abbreviations: CCHF, Crimean-Congo hemorrhagic fever; MERS-CoV, Middle East respiratory syndrome coronavirus; RVF: Rift Valley fever; WNF, West Nile fever; HAV, hepatitis A virus; HEV, hepatitis E virus.

National efforts for forecasting and controling EIDs/RIDs in the EM region, need to be complemented by regional approaches. Population movements are among the most important factors that need to be considered when forecasting and controlling EIDs or RIDs. Most of the EIDs and RIDs mentioned in this study are potentially transmissible during religious pilgrimages where people from across the world gather in Saudi Arabia and Iraq during Hajj and Arba’een, subsequently travelling back to their home countries. Likewise, refugees and displaced persons primarily from Iraq, Afghanistan, Syria, and Yemen have been living under fragile health systems that are unable to detect many of the referenced infectious diseases, or even if detected, do not have the resources to control and/or provide treatment. As a result, when refugees from these countries migrate, various diseases inevitably spread across large regions.

Disasters and wars are further considerations in predicting and monitoring EIDs or RIDs. The ongoing wars in Iraq, Syria, and Yemen have resulted in poor healthcare systems, where previous infrastructures acting as barriers between people and infectious agents have been devastated and therefore contributed to spreading of several diseases. Especially prevalent are food, waterborne, and vector-borne diseases such as cholera, typhoid, dengue fever, leishmaniasis, and plague. As an example, the civil war in Yemen started in March 2015 and has caused more than 2.2 million people to live in shelters with inadequate healthcare services. The damaged infrastructure and poor water and hygiene in the country have created ideal environmental conditions for the spread of infectious diseases leading to an outbreak of dengue fever⁸⁵ and the largest outbreak of cholera in history.¹⁸⁷

Several zoonotic diseases, including MERS, tularemia, Q fever, plague, and RVF, are transferred when an individual is in close contact or lives close to competent vectors and disease hosts. Coordination mechanisms between human and animal health sectors are weak in most countries in the region, so the risk of an increase in zoonotic disease transmission and emergence is present.

Surveillance systems in most countries of the region are not efficient to disseminate the data readily through the routine process. One probable reason can be poor recognition and reporting of some of the referenced diseases such as chikungunya, CCHF, MERS, plague, sandfly fever, tularemia, and WNF by physicians, as cases tend to occur as isolated incidences and sporadically in remote areas.

The WHO estimates that approximately 45% of infectious diseases occur in lower-income populations. For example, Yemen and Egypt have high percentage of poverty and are predisposed to several infectious diseases.^18,85,145 Furthermore, miscommunication or absence of communication in the health system and between countries can result in under-reporting that makes prediction of EIDs and RIDs difficult.

RIDs have recently displayed an upward incidence or prevalence worldwide. For instance, diphtheria outbreaks (in Iran, Pakistan and Sudan), human plague (in Afghanistan and Saudi Arabia), and dengue/dengue hemorrhagic fever (in Pakistan, Egypt, and Sudan) are classified as RIDs in EMR in recent years.^188,189

One of the limitations of this paper is that countries differ in their methods of publishing research papers and reliable documents. The availability of data, studies, and papers may not be congruent between countries. Variation in the capacity of individual countries regarding surveillance and laboratory testing may present further limitations; however, the present review has attempted to provide relatively comprehensive information on the situation of the countries of the region by gathering existing data.

The Way Forward

Development and further strengthening of regional and national capacities for surveillance, laboratory diagnosis, prevention, and control of EIDs and RIDs, in line with requirements of the International Health Regulations (2005), is essential. While the WHO continues to provide guidance and support to all countries to improve preparedness, surveillance, and response to EIDs and RIDs in EMR,¹⁸³ considerable gaps and challenges remain to achieve these capacities.¹⁹⁰ A key strategic consideration for prevention and control of EIDs and RIDs is to establish surveillance capacity for early detection of any occurrences of EIDs or RIDs; as well as the prediction of unexpected occurrence of these high-threat pathogens; and to be able to effectively monitor occurrence patterns of these diseases both nationally and regionally. A wealth of available technology should be implemented in order to help predict, identify, and monitor EIDs or RIDs in the region.^191,192

Other key strategic considerations should include effective coordination and collaboration within and between countries in the region, various scientific fields, and public health institutions to facilitate detection and response to EIDs or RIDs. Collaboration between multiple disciplines through the One Health approach for zoonotic diseases, for example, can lead to early detection, effective response, and better health for people, animals and the environment.¹⁹³ According to the ‘One Health Paradigm’ for global health, the emergence of the majority of new human infectious diseases originates from animal reservoirs. This underscores the need for coordinated surveillance to monitor zoonotic diseases among animals¹⁹⁴ and implementation of preventive One Health Interventions.¹⁰⁶

Campaigns to control mosquito-borne diseases need to focus on clearly explaining why these diseases are a severe problem and how they can be controlled or avoided. Any strategy to further enhance individual and collective consciousness and behavior changes must also address the issues associated with poverty in order to achieve a greater impact.¹⁹⁵

Further studies on EIDs and RIDs such as MERS, CCHF, AHF, and H5N1 are required to understand better the real epidemiological situation of these diseases in the region. This knowledge, alongside understanding other risk factors, can help reduce the risk of disease spread to humans.

It should also be noted that in most cases, due to absence of effective therapeutics or vaccines for most EIDs and RIDs, the governmental will to invest in prevention and control measures for these high-threat pathogens may be lacking in some countries in the region. Research is needed to address these critical knowledge gaps in diagnostic, therapeutic, and preventive measures for most EIDs and RIDs in the region.

Conclusion

The EMR countries are continuously experiencing large population movements associated with the Hajj and Arba’een pilgrimage; internally displaced populations and refugees; and armed groups and transnational migrants. Furthermore, poverty, climate change, alongside the weak public health infrastructure, has predisposed this region to various EIDs and RIDs. Some diseases are endemic in this region and confer threats to international travellers. Several factors are important for the eradication of infectious diseases in this area, including political will, financial investment, cooperative international and local efforts, massive drug administration, vaccination, and surveillance for detection and diagnoses of lower recognized agents.

Understanding and documenting the regional scope and epidemiology of these infectious disease outbreaks will contribute greatly to prevent, rapidly identify, and promptly respond to these health threats in order to minimize deaths, limit geographic spread and interrupt transmission using evidence-based and high value interventions. Developing effective evidence-based public health control measures and intervention strategies to minimize the risk of infection is a key priority for countries in the region (Table 2). Research initiatives to learn more about the nature and impact of infectious diseases in the region are needed for better planning and control measures.

Better targeted investigations should be implemented to identify and prevent widespread emergence and re-emergence of infectious diseases. It is essential to defend the population through multifactorial efforts, including coordinated, well-prepared and well-equipped public health systems alongside partnerships among clinicians, laboratories and public health agencies. Besides, the application of advanced and proper diagnostic methods and surveillance contributes to achieving better results in limited time.

Acknowledgment

We would like to thank Dr. Heba Sobhy Ibrahim Mahrous, from WHO for Eastern Meditation region, Cairo, EGYPT, who supported us in improving the first draft of the manuscript.

Ethical issues

Not applicable.

Competing interests

Authors declare that they have no competing interests.

Authors’ contributions

EM carried out the design of the study. AG and SANM participated in gathering the data, and prepared the first draft of manuscript. All authors critically reviewed the manuscript, applied comments and finalized the manuscript.

Funding

There is no source of funding for this work.

References

1. Woolhouse ME. Population biology of emerging and re-emerging pathogens. Trends Microbiol 2002; 10(10 Suppl):S3-7. doi: 10.1016/s0966-842x(02)02428-9 [Crossref] [ Google Scholar]
2. Petersen E, Petrosillo N, Koopmans M. Emerging infections-an increasingly important topic: review by the Emerging Infections Task Force. Clin Microbiol Infect 2018; 24(4):369-375. doi: 10.1016/j.cmi.2017.10.035 [Crossref] [ Google Scholar]
3. World Health Organization (WHO). The Work of WHO in the Eastern Mediterranean Region: Annual Report of the Regional Director 2014. World Health Organization. Regional Office for the Eastern Mediterranean; 2015.
4. Morens DM, Folkers GK, Fauci AS. The challenge of emerging and re-emerging infectious diseases. Nature 2004; 430(6996):242-249. doi: 10.1038/nature02759 [Crossref] [ Google Scholar]
5. The World Bank. Population, Total. The World Bank; 2018. https://data.worldbank.org/indicator/SP.POP.TOTL. Accessed February 24, 2018.
6. Dabrowski M, De Wulf L. Economic Development, Trade and Investment in the Eastern and Southern Mediterranean Region. SSRN Electronic Journal; 2013. 10.2139/ssrn.2202884.
7. The World Bank. GDP Growth (Annual %). The World Bank; 2016. https://data.worldbank.org/indicator/NY.GDP.MKTP.KD.ZG. Accessed February 24, 2018.
8. McMichael AJ. Global climate change and health: an old story writ large. In: Climate Change and Human Health: Risks and Responses. Geneva, Switzerland: WHO; 2003.
9. Mangold KA, Reynolds SL. A review of dengue fever: a resurging tropical disease. Pediatr Emerg Care 2013; 29(5):665-669. doi: 10.1097/PEC.0b013e31828ed30e [Crossref] [ Google Scholar]
10. Ahmed QA, Arabi YM, Memish ZA. Health risks at the Hajj. Lancet 2006; 367(9515):1008-1015. doi: 10.1016/s0140-6736(06)68429-8 [Crossref] [ Google Scholar]
11. Koçarslan S, Turan E, Ekinci T, Yesilova Y, Apari R. Clinical and histopathological characteristics of cutaneous leishmaniasis in Sanliurfa city of Turkey including Syrian refugees. Indian J Pathol Microbiol 2013; 56(3):211-215. doi: 10.4103/0377-4929.120367 [Crossref] [ Google Scholar]
12. Niazi AU, Jawad MJ, Amirnajad A, Durr PA, Williams DT. Crimean-Congo hemorrhagic fever, Herat province, Afghanistan, 2017. Emerg Infect Dis 2019; 25(8):1596-1598. doi: 10.3201/eid2508.181491 [Crossref] [ Google Scholar]
13. Rauf M, Fatima Tuz Z, Manzoor S, Mehmood A, Bhatti S. Outbreak of chikungunya in Pakistan. Lancet Infect Dis 2017; 17(3):258. doi: 10.1016/s1473-3099(17)30074-9 [Crossref] [ Google Scholar]
14. ProMED-mail. Chikungunya - Sudan (05): (Kassala) cases, health workers, MOH. ProMED-mail 2018; 16 Oct: 20181020.6095579. http://www.promedmail.org. Accessed October 20, 2018.
15. Khalil I, Colombara DV, Forouzanfar MH. Burden of diarrhea in the Eastern Mediterranean Region, 1990-2013: findings from the Global Burden of Disease Study 2013. Am J Trop Med Hyg 2016; 95(6):1319-1329. doi: 10.4269/ajtmh.16-0339 [Crossref] [ Google Scholar]
16. Berger S. Infectious Diseases of Pakistan: 2017 Edition. GIDEON Informatics Inc; 2017.
17. World Health Organization (WHO). Diphtheria Reported Cases. Geneva: WHO; 2019. https://apps.who.int/immunization_monitoring/globalsummary/timeseries/tsincidencediphtheria.html.
18. Kayali G, Kandeil A, El-Shesheny R. Avian influenza A(H5N1) virus in Egypt. Emerg Infect Dis 2016; 22(3):379-388. doi: 10.3201/eid2203.150593 [Crossref] [ Google Scholar]
19. Mockenhaupt FP, Barbre KA, Jensenius M. Profile of illness in Syrian refugees: a GeoSentinel analysis, 2013 to 2015. Euro Surveill 2016; 21(10):30160. doi: 10.2807/1560-7917.es.2016.21.10.30160 [Crossref] [ Google Scholar]
20. Khan NH, Bari AU, Hashim R. Cutaneous leishmaniasis in Khyber Pakhtunkhwa province of Pakistan: clinical diversity and species-level diagnosis. Am J Trop Med Hyg 2016; 95(5):1106-1114. doi: 10.4269/ajtmh.16-0343 [Crossref] [ Google Scholar]
21. Reithinger R, Aadil K, Kolaczinski J, Mohsen M, Hami S. Social impact of leishmaniasis, Afghanistan. Emerg Infect Dis 2005; 11(4):634-636. doi: 10.3201/eid1104.040945 [Crossref] [ Google Scholar]
22. Wagner AL, Mubarak MY, Johnson LE, Porth JM, Yousif JE, Boulton ML. Trends of vaccine-preventable diseases in Afghanistan from the Disease Early Warning System, 2009-2015. PLoS One 2017; 12(6):e0178677. doi: 10.1371/journal.pone.0178677 [Crossref] [ Google Scholar]
23. Alqahtani AS, Rashid H, Basyouni MH, Alhawassi TM, BinDhim NF. Public response to MERS-CoV in the Middle East: iPhone survey in six countries. J Infect Public Health 2017; 10(5):534-540. doi: 10.1016/j.jiph.2016.11.015 [Crossref] [ Google Scholar]
24. Carias C, O’Hagan JJ, Jewett A. Exportations of symptomatic cases of MERS-CoV infection to countries outside the Middle East. Emerg Infect Dis 2016; 22(4):723-725. doi: 10.3201/eid2204.150976 [Crossref] [ Google Scholar]
25. Nowotny N, Kolodziejek J. Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels, Oman, 2013. Euro Surveill 2014; 19(16):20781. doi: 10.2807/1560-7917.es2014.19.16.20781 [Crossref] [ Google Scholar]
26. Leslie T, Whitehouse CA, Yingst S. Outbreak of gastroenteritis caused by Yersinia pestis in Afghanistan. Epidemiol Infect 2011; 139(5):728-735. doi: 10.1017/s0950268810001792 [Crossref] [ Google Scholar]
27. Norris A, Hachey K, Curtis A, Bourdeaux M. Crippling violence: conflict and incident polio in Afghanistan. PLoS One 2016; 11(3):e0149074. doi: 10.1371/journal.pone.0149074 [Crossref] [ Google Scholar]
28. WHO Eastern Mediterranean Region. Polio Eradication Initiative. WHO; 2019. http://www.emro.who.int/polio/countries. Accessed January 16, 2019.
29. Faix DJ, Harrison DJ, Riddle MS. Outbreak of Q fever among US military in western Iraq, June-July 2005. Clin Infect Dis 2008; 46(7):e65-68. doi: 10.1086/528866 [Crossref] [ Google Scholar]
30. Saeed KMI, Ansari J, Asghar RJ, Ahadi J. Concurrent brucellosis and Q fever infection: a case control study in Bamyan province, Afghanistan in 2011. Int J Infect Dis 2012; 16:e37. doi: 10.1016/j.ijid.2012.05.094 [Crossref] [ Google Scholar]
31. Asghar RJ. Hepatitis A and E: not to be forgotten. East Mediterr Health J 2014; 20(3):212-213. [ Google Scholar]
32. Rezig D, Ouneissa R, Mhiri L. [Seroprevalences of hepatitis A and E infections in Tunisia]. Pathol Biol (Paris) 2008; 56(3):148-153. doi: 10.1016/j.patbio.2007.09.026 [Crossref] [ Google Scholar]
33. Bawazir AA, Hart CA, Sallam TA, Parry CM, Beeching NJ, Cuevas LE. Seroepidemiology of hepatitis A and hepatitis E viruses in Aden, Yemen. Trans R Soc Trop Med Hyg 2010; 104(12):801-805. doi: 10.1016/j.trstmh.2010.08.007 [Crossref] [ Google Scholar]
34. Turky AM, Akram W, Al-Naaimi AS, Omer AR, Al-Rawi JR. Analysis of acute viral hepatitis (A and E) in Iraq. Glob J Health Sci 2011; 3(1):70-76. doi: 10.5539/gjhs.v3n1p70 [Crossref] [ Google Scholar]
35. Darwish MA, Faris R, Clemens JD, Rao MR, Edelman R. High seroprevalence of hepatitis A, B, C, and E viruses in residents in an Egyptian village in The Nile Delta: a pilot study. Am J Trop Med Hyg 1996; 54(6):554-558. doi: 10.4269/ajtmh.1996.54.554 [Crossref] [ Google Scholar]
36. Gebreel AO, Christie AB. Viral hepatitis in children: a study in Libya. Ann Trop Paediatr 1983; 3(1):9-11. doi: 10.1080/02724936.1983.11748260 [Crossref] [ Google Scholar]
37. Bouskraoui M, Bourrous M, Amine M. [Prevalence of anti-hepatitis A virus antibodies in chidren in Marrakech]. Arch Pediatr 2009; 16 Suppl 2:S132-136. doi: 10.1016/s0929-693x(09)75317-5 [Crossref] [ Google Scholar]
38. Ghasemian A. Prevalence of hepatitis A across various countries in the Middle East, African and Eastern European countries. Caspian J Intern Med 2016; 7(4):302-303. [ Google Scholar]
39. Pröll S, Nothdurft HD. [The risk of contracting hepatitis A or hepatitis B run by visitors to the Mediterranean and Eastern Europe]. MMW Fortschr Med 2004; 146(20):51-54. [ Google Scholar]
40. Bizri AR, Fares J, Musharrafieh U. Infectious diseases in the era of refugees: hepatitis A outbreak in Lebanon. Avicenna J Med 2018; 8(4):147-152. doi: 10.4103/ajm.AJM_130_18 [Crossref] [ Google Scholar]
41. Miri SM, Alavian SM. Epidemiology of hepatitis a virus infections in Syria, 2017; war and asylum seekers: a global threat. Iran Red Crescent Med J 2017; 19(11):e63622. doi: 10.5812/ircmj.63622 [Crossref] [ Google Scholar]
42. Esmaeilzadeh A, Ganji A, Bahari A, Goshayeshi L. Prevalence of hepatitis E in Iran: a systematic review of the literature. Rev Clin Med 2017; 4(4):152-159. doi: 10.22038/rcm.2017.20169.1187 [Crossref] [ Google Scholar]
43. Kumar RM, Uduman S, Rana S, Kochiyil JK, Usmani A, Thomas L. Sero-prevalence and mother-to-infant transmission of hepatitis E virus among pregnant women in the United Arab Emirates. Eur J Obstet Gynecol Reprod Biol 2001; 100(1):9-15. doi: 10.1016/s0301-2115(01)00448-1 [Crossref] [ Google Scholar]
44. Saad MD, Hussein HA, Bashandy MM. Hepatitis E virus infection in work horses in Egypt. Infect Genet Evol 2007; 7(3):368-373. doi: 10.1016/j.meegid.2006.07.007 [Crossref] [ Google Scholar]
45. Bryan JP, Iqbal M, Tsarev S. Epidemic of hepatitis E in a military unit in Abbotrabad, Pakistan. Am J Trop Med Hyg 2002; 67(6):662-668. doi: 10.4269/ajtmh.2002.67.662 [Crossref] [ Google Scholar]
46. Ayoola EA, Want MA, Gadour MO, Al-Hazmi MH, Hamza MK. Hepatitis E virus infection in haemodialysis patients: a case-control study in Saudi Arabia. J Med Virol 2002; 66(3):329-334. doi: 10.1002/jmv.2149 [Crossref] [ Google Scholar]
47. Madani TA. Alkhumra virus infection, a new viral hemorrhagic fever in Saudi Arabia. J Infect 2005; 51(2):91-97. doi: 10.1016/j.jinf.2004.11.012 [Crossref] [ Google Scholar]
48. Madani TA, Azhar EI, Abuelzein el TM. Alkhumra (Alkhurma) virus outbreak in Najran, Saudi Arabia: epidemiological, clinical, and laboratory characteristics. J Infect 2011; 62(1):67-76. doi: 10.1016/j.jinf.2010.09.032 [Crossref] [ Google Scholar]
49. Al-Tawfiq JA, Memish ZA. Alkhurma hemorrhagic fever virus. Microbes Infect 2017; 19(6):305-310. doi: 10.1016/j.micinf.2017.04.004 [Crossref] [ Google Scholar]
50. Memish ZA, Fagbo SF, Osman Ali A, AlHakeem R, Elnagi FM, Bamgboye EA. Is the epidemiology of alkhurma hemorrhagic fever changing?: a three-year overview in Saudi Arabia. PLoS One 2014; 9(2):e85564. doi: 10.1371/journal.pone.0085564 [Crossref] [ Google Scholar]
51. Carletti F, Castilletti C, Di Caro A. Alkhurma hemorrhagic fever in travelers returning from Egypt, 2010. Emerg Infect Dis 2010; 16(12):1979-1982. doi: 10.3201/eid1612.101092 [Crossref] [ Google Scholar]
52. Musso M, Galati V, Stella MC, Capone A. A case of Alkhumra virus infection. J Clin Virol 2015; 66:12-14. doi: 10.1016/j.jcv.2015.02.019 [Crossref] [ Google Scholar]
53. Horton KC, Fahmy NT, Watany N. Crimean Congo hemorrhagic fever virus and Alkhurma (Alkhumra) virus in ticks in Djibouti. Vector Borne Zoonotic Dis 2016; 16(10):680-682. doi: 10.1089/vbz.2016.1951 [Crossref] [ Google Scholar]
54. Bahgat MM, Kutkat MA, Nasraa MH. Characterization of an avian influenza virus H5N1 Egyptian isolate. J Virol Methods 2009; 159(2):244-250. doi: 10.1016/j.jviromet.2009.04.008 [Crossref] [ Google Scholar]
55. Young SG, Kitchen A, Kayali G, Carrel M. Unlocking pandemic potential: prevalence and spatial patterns of key substitutions in avian influenza H5N1 in Egyptian isolates. BMC Infect Dis 2018; 18(1):314. doi: 10.1186/s12879-018-3222-6 [Crossref] [ Google Scholar]
56. Kammon A, Heidari A, Dayhum A. Characterization of avian influenza and Newcastle disease viruses from poultry in Libya. Avian Dis 2015; 59(3):422-430. doi: 10.1637/11068-032215-ResNote.1 [Crossref] [ Google Scholar]
57. Abubakar A, Elkholy A, Barakat A. Pandemic influenza preparedness (PIP) framework: Progress challenges in improving influenza preparedness response capacities in the Eastern Mediterranean Region, 2014-2017. J Infect Public Health 2020; 13(3):446-450. doi: 10.1016/j.jiph.2019.03.006 [Crossref] [ Google Scholar]
58. World Health Organization (WHO). Cumulative Number of Confirmed Human Cases of Avian Influenza A(H5N1) Reported to WHO (2003-2016). WHO; 2016. http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/. Accessed November 1, 2016.
59. World Health Organization (WHO). Avian Influenza A(H5N1) Situation Update, Egypt, September 2016. WHO; 2016. http://www.emro.who.int/surveillance-forecasting-response/surveillance-news/avian-influenza-ah5n1-situation-update-egypt-september-2016.html. Accessed November 1, 2016.
60. Alkhamis M, Hijmans RJ, Al-Enezi A, Martínez-López B, Perea AM. The use of spatial and spatiotemporal modeling for surveillance of H5N1 highly pathogenic avian influenza in poultry in the Middle East. Avian Dis 2016; 60(1 Suppl):146-155. doi: 10.1637/11106-042115-Reg [Crossref] [ Google Scholar]
61. Khan W, El Rifay AS, Malik M, Kayali G. Influenza research in the Eastern Mediterranean Region: a review. Oman Med J 2017; 32(5):359-364. doi: 10.5001/omj.2017.70 [Crossref] [ Google Scholar]
62. Al-Abri SS, Abdel-Hady DM, Al Mahrooqi SS, Al-Kindi HS, Al-Jardani AK, Al-Abaidani IS. Epidemiology of travel-associated infections in Oman 1999-2013: a retrospective analysis. Travel Med Infect Dis 2015; 13(5):388-393. doi: 10.1016/j.tmaid.2015.08.006 [Crossref] [ Google Scholar]
63. Humphrey JM, Cleton NB, Reusken C, Glesby MJ, Koopmans MPG, Abu-Raddad LJ. Urban chikungunya in the Middle East and North Africa: a systematic review. PLoS Negl Trop Dis 2017; 11(6):e0005707. doi: 10.1371/journal.pntd.0005707 [Crossref] [ Google Scholar]
64. Malik MR, Mnzava A, Mohareb E. Chikungunya outbreak in Al-Hudaydah, Yemen, 2011: epidemiological characterization and key lessons learned for early detection and control. J Epidemiol Glob Health 2014; 4(3):203-211. doi: 10.1016/j.jegh.2014.01.004 [Crossref] [ Google Scholar]
65. Mansoor H. Alarming Rise in Chikungunya Virus Cases in Sindh. DAWN website. https://www.dawn.com/news/1357922. Published September 16, 2017.
66. World Health Organization (WHO). Weekly Epidemiological Monitor. WHO; 2017.
67. Al-Abri SS, Abaidani IA, Fazlalipour M. Current status of Crimean-Congo haemorrhagic fever in the World Health Organization Eastern Mediterranean Region: issues, challenges, and future directions. Int J Infect Dis 2017; 58:82-89. doi: 10.1016/j.ijid.2017.02.018 [Crossref] [ Google Scholar]
68. Wasfi F, Dowall S, Ghabbari T. Sero-epidemiological survey of Crimean-Congo hemorrhagic fever virus in Tunisia. Parasite 2016; 23:10. doi: 10.1051/parasite/2016010 [Crossref] [ Google Scholar]
69. Aziz TA, Ali DJ, Jaff DO. Molecular and serological detection of Crimean-Congo hemorrhagic fever virus in Sulaimani province, Iraq. J Biosci Med 2016; 4(4):36-42. doi: 10.4236/jbm.2016.44006 [Crossref] [ Google Scholar]
70. Al-Abri SS, Hewson R, Al-Kindi H. Molecular epidemiology and high mortality of Crimean-Congo hemorrhagic fever in Oman: a re-emerging infection. bioRxiv 2018:502641. doi: 10.1101/502641 [Crossref]
71. Sahak MN, Arifi F, Saeedzai SA. Descriptive epidemiology of Crimean-Congo Hemorrhagic Fever (CCHF) in Afghanistan: reported cases to National Surveillance System, 2016-2018. Int J Infect Dis 2019; 88:135-140. doi: 10.1016/j.ijid.2019.08.016 [Crossref] [ Google Scholar]
72. Mostafavi E, Haghdoost A, Khakifirouz S, Chinikar S. Spatial analysis of Crimean Congo hemorrhagic fever in Iran. Am J Trop Med Hyg 2013; 89(6):1135-1141. doi: 10.4269/ajtmh.12-0509 [Crossref] [ Google Scholar]
73. Karim AM, Hussain I, Lee JH, Park KS, Lee SH. Surveillance of Crimean-Congo haemorrhagic fever in Pakistan. Lancet Infect Dis 2017; 17(4):367-368. doi: 10.1016/s1473-3099(17)30119-6 [Crossref] [ Google Scholar]
74. Palomar AM, Portillo A, Santibáñez P. Crimean-Congo hemorrhagic fever virus in ticks from migratory birds, Morocco. Emerg Infect Dis 2013; 19(2):260-263. doi: 10.3201/eid1902.121193 [Crossref] [ Google Scholar]
75. Široký P, Bělohlávek T, Papoušek I. Hidden threat of tortoise ticks: high prevalence of Crimean-Congo haemorrhagic fever virus in ticks Hyalomma aegyptium in the Middle East. Parasit Vectors 2014; 7:101. doi: 10.1186/1756-3305-7-101 [Crossref] [ Google Scholar]
76. Al-Abri SS, Hewson R, Al-Kindi H. Clinical and molecular epidemiology of Crimean-Congo hemorrhagic fever in Oman. PLoS Negl Trop Dis 2019; 13(4):e0007100. doi: 10.1371/journal.pntd.0007100 [Crossref] [ Google Scholar]
77. Humphrey JM, Cleton NB, Reusken CB, Glesby MJ, Koopmans MP, Abu-Raddad LJ. Dengue in the Middle East and North Africa: a systematic review. PLoS Negl Trop Dis 2016; 10(12):e0005194. doi: 10.1371/journal.pntd.0005194 [Crossref] [ Google Scholar]
78. Shahhosseini N, Chinikar S, Nowotny N, Fooks AR, Schmidt-Chanasit J. Genetic analysis of imported dengue virus strains by Iranian travelers. Asian Pac J Trop Dis 2016; 6(11):850-853. doi: 10.1016/S2222-1808(16)61144-1 [Crossref] [ Google Scholar]
79. Al Awaidy ST, Khamis F. Dengue fever: an emerging disease in Oman requiring urgent public health interventions. Oman Med J 2019; 34(2):91-93. doi: 10.5001/omj.2019.18 [Crossref] [ Google Scholar]
80. Humphrey JM, Al-Absi ES, Hamdan MM. Dengue and chikungunya seroprevalence among Qatari nationals and immigrants residing in Qatar. PLoS One 2019; 14(1):e0211574. doi: 10.1371/journal.pone.0211574 [Crossref] [ Google Scholar]
81. Doosti S, Yaghoobi-Ershadi MR, Schaffner F. Mosquito surveillance and the first record of the invasive mosquito species Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) in southern Iran. Iran J Public Health 2016; 45(8):1064-1073. [ Google Scholar]
82. Ducheyne E, Tran Minh NN, Haddad N. Current and future distribution of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in WHO Eastern Mediterranean Region. Int J Health Geogr 2018; 17(1):4. doi: 10.1186/s12942-018-0125-0 [Crossref] [ Google Scholar]
83. Bouattour A, Khrouf F, Rhim A, M’Ghirbi Y. First detection of the Asian tiger mosquito, Aedes (Stegomyia) albopictus (Diptera: Culicidae), in Tunisia. J Med Entomol 2019; 56(4):1112-1115. doi: 10.1093/jme/tjz026 [Crossref] [ Google Scholar]
84. Kanani K, Amr Z, Katbeh-Bader A, Arbaji M. First record of Aedes albopictus in Jordan. J Am Mosq Control Assoc 2017; 33(2):134-135. doi: 10.2987/17-6641.1 [Crossref] [ Google Scholar]
85. Alghazali KA, Teoh BT, Loong SK. Dengue outbreak during ongoing civil war, Taiz, Yemen. Emerg Infect Dis 2019; 25(7):1397-1400. doi: 10.3201/eid2507.180046 [Crossref] [ Google Scholar]
86. World Health Organization (WHO). Measles, Fact Sheet. WHO; 2018. http://www.who.int/en/news-room/fact-sheets/detail/measles. Accessed July 10, 2018.
87. Teleb N, Lebo E, Ahmed H. Progress toward measles elimination--Eastern Mediterranean Region, 2008-2012. MMWR Morb Mortal Wkly Rep 2014; 63(23):511-515. [ Google Scholar]
88. World Health Organization (WHO). Measles situation in Eastern Mediterranean Region; in: WHO Regional Office for Eastern Mediterranean Report. Vol 12. Cairo, Egypt: WHO; 2019.
89. Alwan A. The Cost of War. WHO; 2015. http://www.who.int/mediacentre/commentaries/war-cost/en/. Accessed November 26, 2018.
90. ProMED-mail. Measles - Yemen (05): (Amran, Dhamar) fatal, increasing incidence. ProMED-mail 2018; 22 Dec: 20181223.6220714. http://www.promedmail.org. Accessed December 23, 2018.
91. Raad Raad, II II, Chaftari AM, Dib RW, Graviss EA, Hachem R. Emerging outbreaks associated with conflict and failing healthcare systems in the Middle East. Infect Control Hosp Epidemiol 2018; 39(10):1230-1236. doi: 10.1017/ice.2018.177 [Crossref] [ Google Scholar]
92. Mere MO, Goodson JL, Chandio AK. Progress toward measles elimination-Pakistan, 2000-2018. MMWR Morb Mortal Wkly Rep 2019; 68(22):505-510. doi: 10.15585/mmwr.mm6822a4 [Crossref] [ Google Scholar]
93. World Health Organization (WHO). Summary Report on the Meeting of the Eastern Mediterranean Regional Technical Advisory Group [RTAG] on Immunization, Muscat, Oman 14 December 2017. World Health Organization, Regional Office for the Eastern Mediterranean; 2018.
94. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 2012; 367(19):1814-1820. doi: 10.1056/NEJMoa1211721 [Crossref] [ Google Scholar]
95. Hemida MG, Al-Naeem A, Perera RA, Chin AW, Poon LL, Peiris M. Lack of Middle East respiratory syndrome coronavirus transmission from infected camels. Emerg Infect Dis 2015; 21(4):699-701. doi: 10.3201/eid2104.141949 [Crossref] [ Google Scholar]
96. Zumla A, Hui DS, Perlman S. Middle East respiratory syndrome. Lancet 2015; 386(9997):995-1007. doi: 10.1016/s0140-6736(15)60454-8 [Crossref] [ Google Scholar]
97. World Health Organization (WHO). Investigation of Cases of Human Infection with Middle East Respiratory Syndrome Coronavirus (‎‎ MERS-Cov)‎‎: Interim Guidance. WHO; 2018.
98. Al-Abaidani IS, Al-Maani AS, Al-Kindi HS. Overview of preparedness and response for Middle East respiratory syndrome coronavirus (MERS-CoV) in Oman. Int J Infect Dis 2014; 29:309-310. doi: 10.1016/j.ijid.2014.10.003 [Crossref] [ Google Scholar]
99. WHO Eastern Mediterranean Regional office. MERS Situation Update. Vol 10. Cairo, Egypt: WHO; 2017.
100. Poletto C, Boëlle PY, Colizza V. Risk of MERS importation and onward transmission: a systematic review and analysis of cases reported to WHO. BMC Infect Dis 2016; 16(1):448. doi: 10.1186/s12879-016-1787-5 [Crossref] [ Google Scholar]
101. Farag E, Sikkema RS, Vinks T. Drivers of MERS-CoV emergence in Qatar. Viruses 2018; 11(1):22. doi: 10.3390/v11010022 [Crossref] [ Google Scholar]
102. Moniri A, Marjani M, Tabarsi P, Yadegarynia D, Nadji SA. Health care associated Middle East respiratory syndrome (MERS): a case from Iran. Tanaffos 2015; 14(4):262-267. [ Google Scholar]
103. Memish ZA, Zumla AI, Al-Hakeem RF, Al-Rabeeah AA, Stephens GM. Family cluster of Middle East respiratory syndrome coronavirus infections. N Engl J Med 2013; 368(26):2487-2494. doi: 10.1056/NEJMoa1303729 [Crossref] [ Google Scholar]
104. Hunter JC, Nguyen D, Aden B. Transmission of Middle East respiratory syndrome coronavirus infections in healthcare settings, Abu Dhabi. Emerg Infect Dis 2016; 22(4):647-656. doi: 10.3201/eid2204.151615 [Crossref] [ Google Scholar]
105. World Health Organisation. MERS cluster in Wadi Aldwaser, Saudi Arabia Weekly Epidemiological Report 2019;12(7).
106. Farag E, Nour M, Islam MM. Qatar experience on One Health approach for Middle-East respiratory syndrome coronavirus, 2012-2017: A viewpoint. One Health 2019; 7:100090. doi: 10.1016/j.onehlt.2019.100090 [Crossref] [ Google Scholar]
107. Chu DK, Poon LL, Gomaa MM. MERS coronaviruses in dromedary camels, Egypt. Emerg Infect Dis 2014; 20(6):1049-1053. doi: 10.3201/eid2006.140299 [Crossref] [ Google Scholar]
108. Ali M, El-Shesheny R, Kandeil A. Cross-sectional surveillance of Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels and other mammals in Egypt, August 2015 to January 2016. Euro Surveill 2017; 22(11):30487. doi: 10.2807/1560-7917.es.2017.22.11.30487 [Crossref] [ Google Scholar]
109. Mohran KA, Farag EA, Reusken CB. The sample of choice for detecting Middle East respiratory syndrome coronavirus in asymptomatic dromedary camels using real-time reversetranscription polymerase chain reaction. Rev Sci Tech 2016; 35(3):905-911. doi: 10.20506/rst.35.3.2578 [Crossref] [ Google Scholar]
110. Farag EA, Reusken CB, Haagmans BL. High proportion of MERS-CoV shedding dromedaries at slaughterhouse with a potential epidemiological link to human cases, Qatar 2014. Infect Ecol Epidemiol 2015; 5:28305. doi: 10.3402/iee.v5.28305 [Crossref] [ Google Scholar]
111. Yusof MF, Eltahir YM, Serhan WS. Prevalence of Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels in Abu Dhabi Emirate, United Arab Emirates. Virus Genes 2015; 50(3):509-513. doi: 10.1007/s11262-015-1174-0 [Crossref] [ Google Scholar]
112. Conzade R, Grant R, Malik MR. Reported direct and indirect contact with dromedary camels among laboratory-confirmed MERS-CoV cases. Viruses 2018; 10(8). doi: 10.3390/v10080425 [Crossref]
113. Horton DL, McElhinney LM, Freuling CM. Complex epidemiology of a zoonotic disease in a culturally diverse region: phylogeography of rabies virus in the Middle East. PLoS Negl Trop Dis 2015; 9(3):e0003569. doi: 10.1371/journal.pntd.0003569 [Crossref] [ Google Scholar]
114. Abaidani IA, Abri SA, Prakash KP, Hussain MH, Hussain MH, Rawahi AH. Epidemiology of rabies in Oman: a retrospective study (1991-2013). East Mediterr Health J 2015; 21(8):591-597. [ Google Scholar]
115. Bannazadeh Baghi H, Alinezhad F, Kuzmin I, Rupprecht CE. A perspective on rabies in the Middle East-beyond neglect. Vet Sci 2018; 5(3). doi: 10.3390/vetsci5030067 [Crossref]
116. Gautret P, Ribadeau-Dumas F, Parola P, Brouqui P, Bourhy H. Risk for rabies importation from North Africa. Emerg Infect Dis 2011; 17(12):2187-2193. doi: 10.3201/eid1712.110300 [Crossref] [ Google Scholar]
117. Kassir MF, El Zarif T, Kassir G, Berry A, Musharrafieh U, Bizri AR. Human rabies control in Lebanon: a call for action. Epidemiol Infect 2018; 147:1-8. doi: 10.1017/s095026881800300x [Crossref] [ Google Scholar]
118. Outbreak of Rift Valley fever--Saudi Arabia, August-October, 2000. MMWR Morb Mortal Wkly Rep 2000;49(40):905-908.
119. Madani TA, Al-Mazrou YY, Al-Jeffri MH. Rift Valley fever epidemic in Saudi Arabia: epidemiological, clinical, and laboratory characteristics. Clin Infect Dis 2003; 37(8):1084-1092. doi: 10.1086/378747 [Crossref] [ Google Scholar]
120. Awaidy SA, Al Hashami H. Zoonotic diseases in Oman: successes, challenges, and future directions. Vector Borne Zoonotic Dis 2020; 20(1):1-9. doi: 10.1089/vbz.2019.2458 [Crossref] [ Google Scholar]
121. Hassan OA, Ahlm C, Evander M. A need for One Health approach-lessons learned from outbreaks of Rift Valley fever in Saudi Arabia and Sudan. Infect Ecol Epidemiol 2014;4. 10.3402/iee.v4.20710.
122. Hassan OA, Ahlm C, Sang R, Evander M. The 2007 Rift Valley fever outbreak in Sudan. PLoS Negl Trop Dis 2011; 5(9):e1229. doi: 10.1371/journal.pntd.0001229 [Crossref] [ Google Scholar]
123. Fakour S, Naserabadi S, Ahmadi E. The first positive serological study on Rift Valley fever in ruminants of Iran. J Vector Borne Dis 2017; 54(4):348-352. doi: 10.4103/0972-9062.225840 [Crossref] [ Google Scholar]
124. Arsevska E, Hellal J, Mejri S. Identifying areas suitable for the occurrence of Rift Valley fever in North Africa: implications for surveillance. Transbound Emerg Dis 2016; 63(6):658-674. doi: 10.1111/tbed.12331 [Crossref] [ Google Scholar]
125. Downs JW, Flood DT, Orr NH, Constantineau JA, Caviness JW. Sandfly fever in Afghanistan-a sometimes overlooked disease of military importance: a case series and review of the literature. US Army Med Dep J 2017(3-17):60-66.
126. Feinsod FM, Ksiazek TG, Scott RM. Sand fly fever-Naples infection in Egypt. Am J Trop Med Hyg 1987; 37(1):193-196. doi: 10.4269/ajtmh.1987.37.193 [Crossref] [ Google Scholar]
127. Tesh RB, Saidi S, Gajdamovic SJ, Rodhain F, Vesenjak-Hirjan J. Serological studies on the epidemiology of sandfly fever in the Old World. Bull World Health Organ 1976; 54(6):663-674. [ Google Scholar]
128. Cohen R, Babushkin F, Shimoni Z, Shapiro M, Lustig Y. Sandfly virus encephalitis in Israel: two case reports and a review. J Neuroinfect Dis 2017; 8(1):240. doi: 10.4172/2314-7326.1000240 [Crossref] [ Google Scholar]
129. Badakhshan M, Yaghoobi-Ershadi MR, Moin-Vaziri V. Spatial distribution of phlebotomine sand flies (Diptera: Psychodidae) as phlebovirus vectors in different areas of Iran. J Med Entomol 2018; 55(4):846-854. doi: 10.1093/jme/tjy033 [Crossref] [ Google Scholar]
130. Depaquit J, Pesson B, Augot D, Hamilton JG, Lawyer P, Léger N. Proceedings of the IX International Symposium on Phlebotomine Sandflies (ISOPS IX), Reims, France, June 28th-July 1st, 2016. Parasite 2016; 23:E1. doi: 10.1051/parasite/2016051 [Crossref] [ Google Scholar]
131. Shiraly R, Khosravi A, Farahangiz S. Seroprevalence of sandfly fever virus infection in military personnel on the western border of Iran. J Infect Public Health 2017; 10(1):59-63. doi: 10.1016/j.jiph.2016.02.014 [Crossref] [ Google Scholar]
132. Andayi F, Charrel RN, Kieffer A. A sero-epidemiological study of arboviral fevers in Djibouti, Horn of Africa. PLoS Negl Trop Dis 2014; 8(12):e3299. doi: 10.1371/journal.pntd.0003299 [Crossref] [ Google Scholar]
133. Failloux AB, Bouattour A, Faraj C. Surveillance of arthropod-borne viruses and their vectors in the Mediterranean and Black Sea regions within the MediLabSecure Network. Curr Trop Med Rep 2017; 4(1):27-39. doi: 10.1007/s40475-017-0101-y [Crossref] [ Google Scholar]
134. Eybpoosh S, Fazlalipour M, Baniasadi V. Epidemiology of West Nile Virus in the Eastern Mediterranean Region: a systematic review. PLoS Negl Trop Dis 2019; 13(1):e0007081. doi: 10.1371/journal.pntd.0007081 [Crossref] [ Google Scholar]
135. World Health Organization. West Nile fever in Tunisia: update. In: World Health Organization ROfEM, ed. Weekly Epidemiological Monitor. Vol 11. Cairo, Egypt: World Health Organization, Regional Office for Eastern Mediterranean; 2018.
136. Jenabi E, Shirani F, Khazaei S. Alarm of circulating wild poliovirus and of vaccine-derived poliovirus in Middle East countries as a potential risk for re-emerging of polio in Iran. Int J Pediatr 2019; 7(3):9071-9073. doi: 10.22038/ijp.2018.35530.3107 [Crossref] [ Google Scholar]
137. Mbaeyi C, Wadood ZM, Moran T. Strategic response to an outbreak of circulating vaccine-derived poliovirus type 2-Syria, 2017-2018. MMWR Morb Mortal Wkly Rep 2018; 67(24):690-694. doi: 10.15585/mmwr.mm6724a5 [Crossref] [ Google Scholar]
138. Kamadjeu R, Gathenji C. Designing and implementing an electronic dashboard for disease outbreaks response-case study of the 2013-2014 Somalia Polio outbreak response dashboard. Pan Afr Med J 2017; 27(suppl 3):22. doi: 10.11604/pamj.supp.2017.27.3.11062 [Crossref] [ Google Scholar]
139. Martinez M, Shukla H, Ahmadzai M. Progress toward poliomyelitis eradication-Afghanistan, January 2017-May 2018. MMWR Morb Mortal Wkly Rep 2018; 67(30):833-837. doi: 10.15585/mmwr.mm6730a6 [Crossref] [ Google Scholar]
140. Ali M, Lopez AL, You YA. The global burden of cholera. Bull World Health Organ 2012; 90(3):209-218A. doi: 10.2471/blt.11.093427 [Crossref] [ Google Scholar]
141. Bakhshi B, Boustanshenas M, Mahmoudi-aznaveh A. Emergence of Vibrio cholerae O1 classical biotype in 2012 in Iran. Lett Appl Microbiol 2014; 58(2):145-149. doi: 10.1111/lam.12167 [Crossref] [ Google Scholar]
142. Deen J, Mengel MA, Clemens JD. Epidemiology of cholera. Vaccine 2020; 38 Suppl 1:A31-A40. doi: 10.1016/j.vaccine.2019.07.078 [Crossref] [ Google Scholar]
143. Disease outbreaks in Eastern editerranean Region (EMR), January to December 2018. Weekly Epidemiological Monitor. 2018;2018(11):52.
144. Cholera situation in Eastern editerranean Region 2017. Weekly epidemiological monitor. 2018;2018(11):27.
145. Rabaan AA. Cholera: an overview with reference to the Yemen epidemic. Front Med 2019; 13(2):213-228. doi: 10.1007/s11684-018-0631-2 [Crossref] [ Google Scholar]
146. Clarke KEN. Review of the Epidemiology of Diphtheria 2000-2016. Geneva: World Health Organization; 2016.
147. World Health Organization (WHO). Global Health Observatory Data Repository (Eastern Mediterranean Region), Diphtheria Reported Cases by Country. WHO; 2018. http://apps.who.int/gho/data/view.main-emro.1540_41?lang=en.
148. Ceyhan M, Anis S, Htun-Myint L, Pawinski R, Soriano-Gabarró M, Vyse A. Meningococcal disease in the Middle East and North Africa: an important public health consideration that requires further attention. Int J Infect Dis 2012; 16(8):e574-582. doi: 10.1016/j.ijid.2012.03.011 [Crossref] [ Google Scholar]
149. Harrison LH, Pelton SI, Wilder-Smith A. The Global Meningococcal Initiative: recommendations for reducing the global burden of meningococcal disease. Vaccine 2011; 29(18):3363-3371. doi: 10.1016/j.vaccine.2011.02.058 [Crossref] [ Google Scholar]
150. Borrow R, Caugant DA, Ceyhan M. Meningococcal disease in the Middle East and Africa: findings and updates from the Global Meningococcal Initiative. J Infect 2017; 75(1):1-11. doi: 10.1016/j.jinf.2017.04.007 [Crossref] [ Google Scholar]
151. Hausdorff WP, Hajjeh R, Al-Mazrou A, Shibl A, Soriano-Gabarro M. The epidemiology of pneumococcal, meningococcal, and Haemophilus disease in the Middle East and North Africa (MENA) region--current status and needs. Vaccine 2007; 25(11):1935-1944. doi: 10.1016/j.vaccine.2006.11.018 [Crossref] [ Google Scholar]
152. Leimkugel J, Racloz V, da Silva LJ, Pluschke G. Global review of meningococcal disease A shifting etiology. Afr J Bacteriol Res 2009; 1(1):6-18. doi: 10.5897/jbr.9000024 [Crossref] [ Google Scholar]
153. Cabanel N, Leclercq A, Chenal-Francisque V. Plague outbreak in Libya, 2009, unrelated to plague in Algeria. Emerg Infect Dis 2013; 19(2):230-236. doi: 10.3201/eid1902.121031 [Crossref] [ Google Scholar]
154. Tarantola A, Mollet T, Gueguen J, Barboza P, Bertherat E. Plague outbreak in the Libyan Arab Jamahiriya. Euro Surveill 2009; 14(26):19258. [ Google Scholar]
155. Malek MA, Bitam I, Drancourt M. Plague in Arab Maghreb, 1940-2015: a review. Front Public Health 2016; 4:112. doi: 10.3389/fpubh.2016.00112 [Crossref] [ Google Scholar]
156. Esamaeili S, Azadmanesh K, Naddaf SR, Rajerison M, Carniel E, Mostafavi E. Serologic survey of plague in animals, Western Iran. Emerg Infect Dis 2013; 19(9):1549-1551. doi: 10.3201/eid1909.121829 [Crossref] [ Google Scholar]
157. Hashemi Shahraki A, Carniel E, Mostafavi E. Plague in Iran: its history and current status. Epidemiol Health 2016; 38:e2016033. doi: 10.4178/epih.e2016033 [Crossref] [ Google Scholar]
158. Esmaeili S, Naddaf SR, Pourhossein B. Seroprevalence of brucellosis, leptospirosis, and Q fever among butchers and slaughterhouse workers in south-eastern Iran. PLoS One 2016; 11(1):e0144953. doi: 10.1371/journal.pone.0144953 [Crossref] [ Google Scholar]
159. Esmaeili S, Golzar F, Ayubi E, Naghili B, Mostafavi E. Acute Q fever in febrile patients in northwestern of Iran. PLoS Negl Trop Dis 2017; 11(4):e0005535. doi: 10.1371/journal.pntd.0005535 [Crossref] [ Google Scholar]
160. Bailey MS, Trinick TR, Dunbar JA. Undifferentiated febrile illnesses amongst British troops in Helmand, Afghanistan. J R Army Med Corps 2011; 157(2):150-155. doi: 10.1136/jramc-157-02-05 [Crossref] [ Google Scholar]
161. Almogren A, Shakoor Z, Hasanato R, Adam MH. Q fever: a neglected zoonosis in Saudi Arabia. Ann Saudi Med 2013; 33(5):464-468. doi: 10.5144/0256-4947.2013.464 [Crossref] [ Google Scholar]
162. Grace D, Mutua F, Ochungo P, et al. Mapping of Poverty and Likely Zoonoses Hotspots. Nairobi, Kenya: Department for International Development; 2012.
163. Vanderburg S, Rubach MP, Halliday JE, Cleaveland S, Reddy EA, Crump JA. Epidemiology of Coxiella burnetii infection in Africa: a OneHealth systematic review. PLoS Negl Trop Dis 2014; 8(4):e2787. doi: 10.1371/journal.pntd.0002787 [Crossref] [ Google Scholar]
164. Esmaeili S, Gooya MM, Shirzadi MR. Seroepidemiological survey of tularemia among different groups in western Iran. Int J Infect Dis 2014; 18:27-31. doi: 10.1016/j.ijid.2013.08.013 [Crossref] [ Google Scholar]
165. Hepburn MJ, Simpson AJ. Tularemia: current diagnosis and treatment options. Expert Rev Anti Infect Ther 2008; 6(2):231-240. doi: 10.1586/14787210.6.2.231 [Crossref] [ Google Scholar]
166. Rohani M, Mohsenpour B, Ghasemi A. A case report of human tularemia from Iran. Iran J Microbiol 2018; 10(4):250-253. [ Google Scholar]
167. Mostafavi E, Shahraki AH, Japoni-Nejad A. A field study of plague and tularemia in rodents, Western Iran. Vector Borne Zoonotic Dis 2017; 17(4):247-253. doi: 10.1089/vbz.2016.2053 [Crossref] [ Google Scholar]
168. Montagna M, Chouaia B, Pella F. Screening for bacterial DNA in the hard tick Hyalomma marginatum (Ixodidae) from Socotra Island (Yemen): detection of Francisella-like endosymbiont. J Entomol Acarol Res 2012; 44(3):e13. doi: 10.4081/jear.2012.e13 [Crossref] [ Google Scholar]
169. Ghoneim NH, Abdel-Moein KA, Zaher HM. Molecular detection of Francisella spp among ticks attached to camels in Egypt. Vector Borne Zoonotic Dis 2017; 17(6):384-387. doi: 10.1089/vbz.2016.2100 [Crossref] [ Google Scholar]
170. Alvar J, Vélez ID, Bern C. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 2012; 7(5):e35671. doi: 10.1371/journal.pone.0035671 [Crossref] [ Google Scholar]
171. Piroozi B, Moradi G, Alinia C. Incidence, burden, and trend of cutaneous leishmaniasis over four decades in Iran. Iran J Public Health 2019; 48(Suppl 1):28-35. [ Google Scholar]
172. World Health Organization (WHO). Leishmaniasis. WHO; 2018. https://www.who.int/news-room/fact-sheets/detail/leishmaniasis. Accessed December 2018, 2018.
173. Rassi Y, Javadian E, Nadim A. Phlebotomus perfiliewi transcaucasicus, a vector of Leishmania infantum in northwestern Iran. J Med Entomol 2009; 46(5):1094-1098. doi: 10.1603/033.046.0516 [Crossref] [ Google Scholar]
174. AlSamarai AM, AlObaidi HS. Cutaneous leishmaniasis in Iraq. J Infect Dev Ctries 2009; 3(2):123-129. doi: 10.3855/jidc.59 [Crossref] [ Google Scholar]
175. Khatri ML, Di Muccio T, Fiorentino E, Gramiccia M. Ongoing outbreak of cutaneous leishmaniasis in northwestern Yemen: clinicoepidemiologic, geographic, and taxonomic study. Int J Dermatol 2016; 55(11):1210-1218. doi: 10.1111/ijd.13310 [Crossref] [ Google Scholar]
176. Aoun K, Bouratbine A. Cutaneous leishmaniasis in North Africa: a review. Parasite 2014; 21:14. doi: 10.1051/parasite/2014014 [Crossref] [ Google Scholar]
177. Ali A, Ur Rehman T, Qureshi NA, Ur Rahman H. New endemic focus of cutaneous leishmaniasis in Pakistan and future epidemics threats. Asian Pac J Trop Dis 2016; 6(2):155-159. doi: 10.1016/S2222-1808(15)61003-9 [Crossref] [ Google Scholar]
178. Khalil MI, Bahnass MM, Abdallah MIM. Epidemiological and serological study of leishmaniasis in Najran Region, Saudi Arabia. J Biol Life Sci 2017; 8(1):59-71. doi: 10.5296/jbls.v8i1.10793 [Crossref] [ Google Scholar]
179. Al-Salem WS, Pigott DM, Subramaniam K. Cutaneous leishmaniasis and conflict in Syria. Emerg Infect Dis 2016; 22(5):931-933. doi: 10.3201/eid2205.160042 [Crossref] [ Google Scholar]
180. Rehman K, Walochnik J, Mischlinger J, Alassil B, Allan R, Ramharter M. Leishmaniasis in northern Syria during civil war. Emerg Infect Dis 2018; 24(11):1973-1981. doi: 10.3201/eid2411.172146 [Crossref] [ Google Scholar]
181. Du R, Hotez PJ, Al-Salem WS, Acosta-Serrano A. Old world cutaneous leishmaniasis and refugee crises in the Middle East and North Africa. PLoS Negl Trop Dis 2016; 10(5):e0004545. doi: 10.1371/journal.pntd.0004545 [Crossref] [ Google Scholar]
182. ProMED-mail. Leishmaniasis, cutaneous - Libya: (MR), 2018; 13 April: 20180413.5742538. http://www.promedmail.org. Accessed April 10, 2018.
183. Buliva E, Elhakim M, Tran Minh NN. Emerging and reemerging diseases in the World Health Organization (WHO) Eastern Mediterranean Region-progress, challenges, and WHO initiatives. Front Public Health 2017; 5:276. doi: 10.3389/fpubh.2017.00276 [Crossref] [ Google Scholar]
184. World Health Organization (WHO). Summary Report on the Intercountry Meeting on the Strategic Framework for Prevention and Control of Emerging and Epidemic-Prone Diseases in the Eastern Mediterranean Region, Amman, Jordan 16-19 December 2018. World Health Organization. Regional Office for the Eastern Mediterranean;2019.
185. WHO Regional Office for the Eastern Mediterranean. Strategic framework for the prevention and control of emerging and Epidemic-Prone diseases in the Eastern Mediterranean Region. WHO Regional Office for the Eastern Mediterranean; 2019.
186. Annual disease outbreak reports, Infectious disease outbreaks reported in the Eastern Mediterranean Region in 2016, 2017, and 2018. http://www.emro.who.int/pandemic-epidemic-diseases/information-resources/annual-disease-outbreak-reports.html.
187. Federspiel F, Ali M. The cholera outbreak in Yemen: lessons learned and way forward. BMC Public Health 2018; 18(1):1338. doi: 10.1186/s12889-018-6227-6 [Crossref] [ Google Scholar]
188. Aungkulanon S, McCarron M, Lertiendumrong J, Olsen SJ, Bundhamcharoen K. Infectious disease mortality rates, Thailand, 1958-2009. Emerg Infect Dis 2012; 18(11):1794-1801. doi: 10.3201/eid1811.120637 [Crossref] [ Google Scholar]
189. Christou L. The global burden of bacterial and viral zoonotic infections. Clin Microbiol Infect 2011; 17(3):326-330. doi: 10.1111/j.1469-0691.2010.03441.x [Crossref] [ Google Scholar]
190. WHO Regional Office for the Eastern Mediterranean, Implementation of the IHR 2005 in the Region with focus on Ebola virus diseases. East Mediterr Health J. 2015;21(10):773-775.
191. Milinovich GJ, Williams GM, Clements AC, Hu W. Internet-based surveillance systems for monitoring emerging infectious diseases. Lancet Infect Dis 2014; 14(2):160-168. doi: 10.1016/s1473-3099(13)70244-5 [Crossref] [ Google Scholar]
192. Brownstein JS, Freifeld CC, Madoff LC. Digital disease detection--harnessing the Web for public health surveillance. N Engl J Med 2009; 360(21):2153-2155. doi: 10.1056/NEJMp0900702 [Crossref] [ Google Scholar]
193. Seimenis A, Battelli G. Main challenges in the control of zoonoses and related foodborne diseases in the South Mediterranean and Middle East region. Vet Ital 2018; 54(2):97-106. doi: 10.12834/VetIt.1340.7765.1 [Crossref] [ Google Scholar]
194. Mahrous H, Redi N, Nguyen TMN, Al Awaidy S, Mostafavi E, Samhouri D. One Health operational framework for action for the Eastern Mediterranean Region, focusing on zoonotic diseases. East Mediterr Health J 2020; 26(6):720-725. doi: 10.26719/emhj.20.017 [Crossref] [ Google Scholar]
195. Bandura A. The social and policy impact of social cognitive theory. In: Mark MM, Donaldson SI, Campbell B, eds. Social Psychology and Evaluation. The Guilford Press; 2011:33-70.
196. Alvar J, Vélez ID, Bern C. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 2012; 7(5):e35671. doi: 10.1371/journal.pone.0035671 [Crossref] [ Google Scholar]
197. Almogren A, Shakoor Z, Hasanato R, Adam MH. Q fever: a neglected zoonosis in Saudi Arabia. Ann Saudi Med 2013; 33(5):464-468. doi: 10.5144/0256-4947.2013.464 [Crossref] [ Google Scholar]
198. Zargar A, Maurin M, Mostafavi E. Tularemia, a re-emerging infectious disease in Iran and neighboring countrie. Epidemiol Health 2015; 37:e2015011. doi: 10.4178/epih/e2015011 [Crossref] [ Google Scholar]