Abstract
After the Arab Spring uprising, Syria descended into a civil war in 2011. By March 2016, the United Nations reported that 13.5 million Syrians required humanitarian assistance, including 6.6 million internally displaced persons and more than 4.8 million refugees outside of Syria. Turkey is currently hosting the largest number of Syrian refugees—more than 2.7 million. A limited number of refugees are living in camps settled around the border, and others are spread throughout Turkey. This explosive and unexpected increase in the Syrian population in Turkey has had several negative impacts on health and social determinants. The overload of healthcare facilities has led to shortages in childhood immunization programs, drugs, and access to clean water and food supplies. According to Ministry of Health data, more than 7.5 million Syrians were examined at outpatient clinics, and 299,240 were hospitalized; most of those hospitalized were injured and wounded victims who require and have been occupying intensive care units. The refugees generally live in crowded and unsanitary conditions, which may lead to the spread of respiratory, skin, gastrointestinal, and genital system infections. Currently, measles, poliomyelitis, leishmaniasis, and multidrug-resistant tuberculosis are the reemerging infections being most frequently recorded. Multidrug-resistant gram-negative bacterial infections seem to be an increasing problem in gunshot or surgical wounds. Hepatitis A, malaria, and varicella have been seen with a high incidence among the refugees. There are many problems waiting to be resolved for health and living standards in Turkey.
As of this spring, the United Nations reported that 13.5 million Syrians required humanitarian assistance, including 6.6 million internally displaced persons and more than 4.8 million refugees outside of Syria. Turkey is currently hosting the largest number of Syrian refugees—more than 2.7 million. This explosive and unexpected increase in the Syrian population in Turkey has led to an overload of healthcare facilities, shortages in childhood immunization programs and drugs, and lack of access to clean water and food supplies. Many refugees live in crowded and unsanitary conditions, leading to the spread of respiratory, skin, gastrointestinal, and genital system infections. Measles, poliomyelitis, leishmaniasis, and multidrug-resistant tuberculosis are the reemerging infections being most frequently recorded.
D
For the preparation of this article, reviews, case series, and case reports about Syrian refugees from the World Health Organization (WHO), UNHCR, the Republic of Turkey Prime Ministry of Disaster and Emergency Management Presidency (AFAD), and the Turkish Ministry of Health were reviewed. PubMed and the Web of Science databases were searched with the terms “Syrian, refugees, Turkey.”
Turkey is receiving many refugees not only from Syria but also from Iraq, Iran, Afghanistan, Pakistan, and Central Asian Turkic Countries. Since the onset of the Syrian conflict in 2011, hundreds of thousands of civilians have been wounded and more than 200,000 Syrians have been killed as of the end of 2015. 3 Thousands of Syrians have been forced to escape and have been displaced from their homes. While the Syrian population was 22,198,110 in 2010, in 2016 it is estimated to be 17,951,640. Because of the ongoing civil war, Syria's population has gradually decreased. As of February 2016, the United Nations has identified 13.5 million Syrians requiring humanitarian assistance, including 6.6 million internally displaced within Syria and more than 4.8 million outside of Syria.
Turkey is one of the largest host countries, with more than 2.7 million Syrian refugees as of March 2016 (Table 1).1,4 There are 300,000 refugees living in camps located in Syrian border cities (Sanliurfa, Gaziantep, Kilis, Hatay, Kahramanmaras, Adiyaman, Adana, and Osmaniye). There are also 2,440,000 refugees living outside of camps, who are spread throughout Turkey from the south through central and western cities including Istanbul, Ankara, and Izmir (Table 2).2,4,5
Syrian Refugees, March 2016
Age and Gender Distribution of Syrian Refugees in Turkey
The Syrian health system has deteriorated since the beginning of the civil war. It is noted that many Syrian hospitals and medical facilities have been destroyed by fighter jet strikes and bombing, resulting in the death of many doctors, nurses, and other medical staff. Since the conflict began in 2011, Physicians for Human Rights has recorded 679 medical personnel killed. They have also documented that some personnel were killed in bombings at their hospitals or clinics, some were shot dead, and at least 157 were executed or tortured to death.6,7
Because of the loss of infrastructure in Syrian hospitals and the lack of medical personnel, wounded civilians and fighters have been transferred to Turkish hospitals. According to the Turkish Ministry of Health and AFAD records, between 2011 and 2015, Syrian refugees seen for care included outpatient health examinations (7,519,668), hospitalizations (302,805), wounded patient admission (25,467), surgical operations (228,537), and childbirths (≈60,000). The total health cost of Syrian refugees was 2,860,716,693.89 Turkish liras ($883,005,756.51) at the end of 2015.8,9 Since 2011, Turkey has spent over $20 billion ($10 billion spent by the government and $10 billion spent by nongovernmental organizations) for Syrian refugees on direct assistance (Recep Tayyip Erdogan, President of the Republic of Turkey, announced this at the opening lecture of the World Humanitarian Summit 23-24 May 2016, Istanbul, Turkey). More than 90% of Syrian refugees living in camps use health services,4,5 as healthcare facilities are located in the camps. Outside of the camp, healthcare service use is lower: Only 60% of the refugees living out of the camps used Turkish health services. The low percentage of health services use among the Syrian refugees living out of the camps may be attributed to insufficient information, communication barriers, or lack of the government-issued identification number necessary to use health services in Turkey.2,4,5 Currently, the large number of refugees in Turkey has had an effect on public security, budget overload, strain on the health service system, and an increased cost of living.
Acute Care of Wounded
Thousands of seriously injured patients from Syria have been transferred to Turkey for surgical intervention and intensive care monitoring. The documentation showed that patients had been injured with gunshots, explosives, and shrapnel, were victims of accidental trauma, and had wounds due to having been beaten or stabbed.10-13 The mean cost per hospital admission was estimated to be US$1,000 to US$1,500. On the other hand, seriously injured and complicated cases needed intensive care support, which increased the average cost. 14 After a patient is discharged, he or she needs a period of rehabilitation therapy and other supportive services, which can be lengthy.
Nosocomial Antibiotic-Resistant Bacterial Infections
Antibiotic resistance is a global healthcare challenge. The refugees coming across international borders can disseminate unusual and drug-resistant microorganisms. The acute care of war wound infections contributes to the emergence of antimicrobial resistance in several ways. A prolonged hospital stay, wide use of antimicrobials, and/or multiple surgical interventions may increase the development of multidrug-resistant bacteria. Nosocomial transmission is also an important factor in the spread of multidrug-resistant microorganisms in hospital intensive care or other units.15-18 Reinheimer et al 16 reported that the prevalence of multidrug-resistant gram-negative bacteria in refugees was 4-fold higher than in resident patients in Germany. In a microbiological surveillance study in Italy, a large number of unusual gram-negative bacteria species had been isolated from swabs taken from 48 Syrian refugees upon their arrival in Italy. Among these isolates, gram-negative bacterial strains resistant to carbapenems and/or extended-spectrum beta lactamase producers and methicillin-resistant gram-positive cocci were detected. 17 Carbapenem-resistant Acinetobacter baumannii strains carrying the blaNDM-1 gene have been reported in 2 patients in Adana. One patient was a 49-year-old female Syrian refugee hospitalized with acute renal failure and chronic gastritis; the second case was a 67-year-old woman living in Adana, who had been hospitalized due to motor neuron diseases in the neurological ICU in 2014. 18 An unusual nosocomial outbreak of orf infection, which is caused by parapoxvirus, was reported in a hospital burn unit in Gaziantep, Turkey; this outbreak involved 13 burn patients, including 3 Syrian refugees. 19
Community-Acquired Infections and Outbreaks
A refugee's lifestyle is often quite challenging because of the lack of basic requirements such as shelter, food, and water. Thus, refugees can be highly susceptible to infections for various reasons, including living outdoors in open areas, exposure to extreme (warm and cool) temperatures, crowded and unsanitary living conditions, low standards of environmental hygiene, unsafe food and water, starvation, interrupted immunization programs, a lack of infection control and prevention in local healthcare settings, and limited to access health care. For these reasons, refugees are prone to bacterial and viral respiratory system infections, including influenza, measles, mumps, tuberculosis and meningococcal infections, gastrointestinal system infections, skin and soft tissue infections, sexually transmitted infections, ectoparasites, and vector-borne infections.20-22 WHO has also warned that a cholera outbreak has arisen in Iraq, which is a potential threat to all nearby crisis areas. 23 Table 3 shows the communicable diseases in Syrian refugees between 2012 and 2015 recorded by the Public Health Service.
Communicable Diseases in Syrian Refugees Between 2012 and 2015 Recorded by Ministry of Health
The Syrian conflict has led to reemerging infections in Turkey, including measles, tuberculosis, cutaneous leishmaniasis, and poliomyelitis.
Measles
Measles is a highly contagious viral disease that is transmitted by the respiratory route. It is preventable by vaccination. Currently, the disease is reemerging in some countries where measles was previously controlled because of the break in scheduled vaccinations caused by uncontrolled migration, fighting, poverty, and the heavy work load of the health services system.24,25 The measles vaccine is routinely given in the 12th month and 6th year, and currently 94% of children in Turkey have been vaccinated. 26 From 2006 to 2010, 3 to 7 measles cases were recorded by the Turkish Public Health Service. Since 2011, measles has been on the rise among Syrian refugees in Turkey. Measles was reported in 111 Syrian refugees in 2011, 31 in 2012, 674 in 2013, and 114 in 2014. The Public Health Service has initiated vaccination against measles in the refugee camps in Turkey.20,21,26
Tuberculosis
As is well known, tuberculosis is a socioeconomic disease. Armed or civil wars, disasters, poor nutrition, lack of food, and poverty have had a negative impact on the control of tuberculosis. It is noted that 10,689 Syrian refugees were screened for tuberculosis, and the prevalence was found to be 18.7/100,000 in Turkey. In 2015, 558 new cases among Syrian refugees were diagnosed and treated.20,21,26 Figure 1 shows the appearance of disseminated pulmonary tuberculosis in a chest X-ray of a 19-year-old female Syrian refugee who was married with a 2-year-old child. The patient was successfully treated.
Chest X-ray of a 19-year-old female Syrian refugee diagnosed with tuberculosis
Cutaneous Leishmaniasis
Cutaneous leishmaniasis is an endemic protozoan infection in Middle Eastern countries, including Syria and the southeast region of Turkey that neighbors Syria. 27 A total of 46,003 new cases were reported in Turkey between 1990 and 2010. Of these cases, 96% had originated from the neighboring Syrian cities. 28 A total of 5,495 cases of cutaneous leishmaniasis among Syrian refugees was recorded by the Public Health Service of the Turkish Ministry of Health between 2012 and 2015 (Table 3). It is also noted that an increase has been seen in Turkish domestic cases. 26
Poliomyelitis
Although Syria has declared itself polio free for the past 15 years, it is noted that 37 cases of poliomyelitis were reported through 2013. 29 Because of the ongoing conflict, more than 2 million children could not be vaccinated. 30 This situation prompted the need for polio vaccination in Turkey. Polio vaccination was started for all Syrian children before they entered the camps and for 1 million Turkish children under the age of 5 in 7 provinces that are located near the Syrian border. Up to now, no polio cases have been reported.4,20 Measles, mumps, and rubella (MMR), tetanus, and diphtheria vaccinations are provided to all Syrian children living inside or outside of camps. 26
Mental and Physical Rehabilitation
For anyone, displacement from home or becoming a refugee causes serious psychological trauma. 31 Communication barriers place additional stress on refugees. In addition, being away from home and facing uncertainty for the future, physical stresses, trauma, or wounds of war also have a negative psychological impact. Psychologically traumatized people need treatment, rehabilitation, and assistance with adaptation to their new life in Turkey.9,32,33 According to a study published by WHO in 2010, many people have suffered from sadness (60%), desperation, loneliness, and anxiety (50%) during the war in Syria. 34 In 2014, WHO estimated that 600,000 Syrians had severe mental disorders. 30 Unfortunately, many refugees will not be able to reach mental health services in Syrian neighboring countries and will have to live with their mental disorders and deal with their economical and housing problems.
Biosecurity
The Syrian civil war is one of the worst humanitarian disasters since World War II. It has claimed more than 200,000 casualties, including more than 8,000 documented deaths of children under the age of 18. 35 A huge group of people has been displaced internally or have become refugees in Syria. This conflict affected not only Syria but also neighboring and European countries. Host countries faced with this humanitarian crisis were unprepared to deal with it. Host countries have been required to provide protection, shelter, safe food and water, health services, education for children, rehabilitation of wounded people, and employment. And the large number of refugees in Turkey has had an effect on public security, sometimes leading to conflict with Turkish people in hospitals or in the community.1,2,4,5,9,14
Since the beginning of the Syrian crisis, infections have reemerged in Turkey, including multidrug-resistant gram-negative bacterial infections, tuberculosis, measles, leishmaniasis, diarrheal diseases, and hepatitis A. There is also great risk for poliomyelitis and cholera outbreaks in the southeast region of Turkey, as has been seen in the camps in Iraq and Syria.18-21,28,29 Refugees living in urban and rural areas in southeastern Turkey may be at risk of exposure to vector-borne diseases such as malaria and other tropical diseases. Crowded living conditions, living in rural areas, and changes in eco-biology due to global warming all may contribute to the reemergence of West Nile virus infection, which was seen previously in Turkey.36,37 The last plague outbreak was recorded in Akcakale, a town located on the Turkish-Syrian border, in 1947; this outbreak involved 32 cases.38,39 As many refugees are settled in camps or out of camps near the Turkish-Syrian border and some groups are living in urban and rural areas, there is the potential for a plague outbreak to occur.
Currently, many religious, ethnic, separatist, and leftist terrorist groups are active in Middle Eastern countries. The Turkish-Syrian border has remained unprotected and difficult to control, because of a large number of Syrian refugees being forced to cross the border through Turkey. Potentially, terrorist groups could cross the border with the refugees. During the ongoing refugee crisis, Turkey has incurred many casualties with explosive terrorist attacks in Ankara, Istanbul, and in the Turkish-Syrian border cities.40,41 In association with terrorist activity, there is concern about the intentional use of biologic agents to cause harm. On the night of August 21, 2013, a nerve agent (sarin gas) was reportedly dispersed in Syria. More than 1,400 civilians were killed and thousands of others have been affected. 42 Following this event, rumors that smallpox virus and Bacillus anthracis spores could be used as terrorist agents have spread throughout the Middle Eastern countries, including Turkey. In preparation of their biodefense systems, countries should consider countermeasures against biological agents.
In addition to these challenges to the Turkish healthcare system, Turkish healthcare providers currently have a large number of Syrian refugee patients with whom they have difficulty communicating because of language barriers and the fact that the patients have no medical records. These patients are profoundly affected both socially and psychologically by the trauma they have experienced during their flight from Syria.
While the Turkish people and government are committed to providing social and medical care for the Syrian refugees, the additional health cost and excessive demands on the healthcare system are straining Turkey's healthcare resources. International collaboration is a key factor in dealing with healthcare and residency problems and preventing a terrorist attack.