ISSN: 2474-3658

Isaac et al. J Infect Dis Epidemiol 2020, 6:172

DOI: 10.23937/2474-3658/1510172
Volume 6 | Issue 6
Journal of Open Access

Infectious Diseases and Epidemiology

Literature Review

Infectious Diseases in Times of Conflict and War: The Loyal

Companions
Isaac I1, Malaeb M1, Bou khalil A1, Musharrafieh U2,3* and Bizri AR3,4
Check for
updates
1Department of Internal Medicine, American University of Beirut Medical Center, Beirut, Lebanon
2Department of Family Medicine, American University of Beirut Medical Center, Beirut, Lebanon
3Division of Infectious Diseases, Department of Internal Medicine, American University of Beirut Medical Center, Beirut,
Lebanon
4Conflict Medicine Program, Global Health Institute, American University of Beirut, Beirut, Lebanon

*Corresponding authors: Umayya Mousharafieh, MD, Department of Family Medicine, American University of Beirut
Medical Center, Beirut, Lebanon, Tel: +961-1-350-000, Ext: 3042

Abstract sanitary infrastructure, and over stretched public health as-

sets, when combined together, may lead to increase and
The association between war, conflict, massive force dis- spread of infectious diseases.
placement and infectious diseases has long been estab-
lished. The influx of large numbers of syrian refugees to Abbreviations
Lebanon burdened the country’s infrastructure on several
LMoPH-EUS: Lebanese Ministry of Public Health- Epidemi-
levels, including the public health sector. The aim of this arti-
ological Surveillance Unit; AIDS: Acquired Immunodeficien-
cle is to evaluate the association between certain reportable
cy Syndrome; UNCHR: United Nations High Commissioner
infectious diseases, and the presence of Syrian refugees in
for Refugees; NTP: National Tuberculosis Program; WHO:
Lebanon. Data, from non-governmental organizations and
World Health Organization; HAV: Viral Hepatitis A; HBV:
the Lebanese Ministry of Public Health- Epidemiological
Viral Hepatitis B; HCV: Viral Hepatitis C; IgG: Immunoglob-
Surveillance Unit, National AIDS Program and National Tu-
ulin G; UNICEF: The United Nations International Children
berculosis Program was reviewed. Information about Syr-
Fund; USAID: United States Agency for International De-
ian refugees, when available, was compared to Lebanese
velopment; IOM: International Organization for Migration;
nationals. Several search engines were utilized to obtain
MMR: Measles, Mumps, Rubella; USA: United States of
literature relevant to infectious diseases associated with the
America; CDC: Center for Disease Control and prevention;
presence of syrian refugees in Lebanon. For certain infec-
TB: Tuberculosis; MDR-TB: Multidrug resistance Tubercu-
tions mainly tuberculosis treatment was provided to both
losis
the host and refugee communities. Whereas treatment for
other infections such as viral hepatitis and brucellosis, was
only available to the host community and not the refugees. Introduction and Background
Leishmaniasis outbreaks were exclusively linked to the
presence of Syrian refugees and treatment was provided The total number of Syrian refugees in Lebanon,
to the refugees to protect the host community. Outbreaks of registered with the United Nations High Commissioner
vaccine preventable diseases were managed through inten-
sification and better outreach of immunization campaigns
for Refugees (UNCHR), exceeded 1 million in 2016. It is
for both communities. The measles, mumps, and viral hepa- believed that more than 40% of the Syrian refugees re-
titis A outbreaks were partially attributed to the extra burden siding in Lebanon are non-registered leading to a total
due to the presence of large numbers of refugees and their estimate of about 1.5 million [1]. This makes Lebanon
distribution in Lebanon. the country with the highest number of refugees per
Significant risks from transmissible infectious diseases to capita in the world [2]. Syrians began fleeing to Lebanon
both the host community and refugees exist in connection as early as 2011, where the majority of these refugees,
with the Syrian crises. War, crisis, overcrowding, suboptimal
were not located in camps or tented settlements but

Citation: Isaac I, Malaeb M, Bou khalil A, Musharrafieh U, Bizri AR (2020) Infectious Diseases in Times
of Conflict and War: The Loyal Companions. J Infect Dis Epidemiol 6:172. doi.org/10.23937/2474-
3658/1510172
Accepted: November 02, 2020: Published: November 04, 2020
Copyright: © 2020 Isaac I, et al. This is an open-access article distributed under the terms of the
Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited.

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DOI: 10.23937/2474-3658/1510172 ISSN: 2474-3658

rather spread all over the country [3]. This article will [4]. Syrian refugees represented 14% to 18% of all re-
discuss the effect of the presence of these refugees on ported cases between 2013 and 2018 [3].
certain reportable infectious diseases in Lebanon.
The host community, as well as the refugees, suffer
Methodology from deterioration in their livelyhood where, according
to the International Labor Organization, around 170,000
A descriptive analysis was conducted to review the Lebanese citizens has fallen below poverty line by 2015,
incidence of certain reportable infectious diseases be- while unemployment rate increased to 20%. This wors-
tween 2008 and 2019. Data rom the Lebanese Minis- ening in living conditions along with the absence of san-
try of Public Health -Epidemiological Surveillance Unit itary infrastructure in Syrian refugees concentration ar-
(LMoPH-ESU), and National Tuberculosis Program (NTP) eas and poor sanitary infrastructure in the country might
[3] was reviewed during the study period relevant to have facilitated the spread of the virus. The unusual dry
viral hepatitis A, B and C, measles, mumps, salmonel- weather and the drop in annual rain precipitation by
losis, brucellosis, tuberculosis, and leishmaniasis. In- more than half the yearly average can be another con-
formation about incidence over years among the pop- tributing factor [5]. As a result of this increase in HAV in-
ulation in general and Syrian refugees when available cidence, the Lebanese health authorities recommended
was obtained. A PubMed, EMBASE, Google Scholar, and the introduction HAV vaccination to the national immu-
COCRHANE database literature search was conducted nization calendar. Lebanon has not integrated the vac-
using Lebanon, Syria, viral hepatitis A, B and C, measles, cine against HAV earlier because only countries with ep-
mumps, salmonella, brucella, tuberculosis, leishmania- idemiological shift in HAV from endemic to intermediate
sis, and refugees as key words. Results were discussed endemicity were advised to do so [6]. Lebanon commu-
pertinent to each infectious disease entity and conclu- nicated the problem to the 67th World Health Assembly
sions were drawn for the overall situation. where a new resolution for HAV was set that includes
plans to improve actions related to health promotion
Viral Hepatitis A (HAV) and prevention of viral hepatitis, encouraging and rein-
HAV is endemic in both Lebanon and Syria. A drop in forcing immunization strategies [7]. The United Nations
HAV IgG sero-prevalence from 97.7% to 78% between International Children Fund (UNICEF) and United States
1982 and 2005 among Lebanese adults was document- Agency for International Development (USAID) provided
ed, rendering them more susceptible to symptomatic help for the country in improving and guarantying citi-
clinical illness [4]. Since 2013, Lebanon experienced a zens access to inexpensive, safe and reliable water [8].
major rise in the annual incidence of reported HAV in- Figure 1 reveals trends in the incidence of HAV reported
fections from 5-18/100000 up to 34/100000 inhabitants cases between 2008 and 2018.

Figure 1: The reported HAV cases to LMoPH-ESU from 2008 till 2018 including Lebanese nationals and Syrian refugees.

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Figure 2: The reported cases of HBV infection to LMoPH-ESU from 2008 till 2018 including Lebanese nationals and Syrian
refugees.

Viral Hepatitis B (HBV) it difficult to assess its impact and potential complica-
tions. The LMoPH provides free immunization coverage,
The prevalence of HBV in Lebanon is 1.74% [9] as
including HBV vaccines, for children of Syrian refugees
compared to 5.6% in Syria before the war [10]. The av-
similar to that of the Lebanese children [14].
erage annual number of reported cases to the LMPH-
ESU between 2008 and 2018 is 250 (Figure 2). An aver- Viral Hepatitis C (HCV)
age number of 38 cases per year was reported among
Two main genotypes of HCV predominate in the Mid-
Syrian refugees residing in the country between 2013
dle East region G4 and G1 [15]. The prevalence of HCV in
and 2018. According to studies from blood banks car-
the general population is estimated to be around 0.2%
ried out by the Syrian Ministry of Health, HBV seroprev-
in Lebanon and 0.4% in Syria. Among the lebanese na-
alence was 2.66% and the vaccination rate was 83% in
tionals the distribution of genotypes suggests that G1 is
2008. In 2011, with the start of the Syrian war, sero-
the most prevalent (39.9%), followed by G4 (32.1%). As
prevalence was 1.75% and HBV vaccination coverage
for the Syrian population G4 is most common (58.2%)
rates dropped to 69% [10,11]. In a study at GeoSentinel
followed by G1 (29.5%) [16]. In Turkey, the seropreva-
clinics conducted in eight countries between June 2011
lence of HCV among Syrian refugee children was 1.8% as
and November 2015, the status of hepatitis B and C was
compared 0.1% in Turkish children [13]. The seroprev-
examined in 44 adult Syrian refugees, HBV infection was
alence of hepatitis C at the GeoSentinel clinics was 2%
documented in 6.8% indicating that screening protocols
which accords with the turkish data and the expected
for adults should address this infection and allocate the
range already known in Syria [12].
resources need for screening, treatment and follow-up
[12]. A retrospective review of data was conducted be- The new directly acting anti-retroviral agents are
tween April 2014 and December 2015 in Turkey on 171 dispensed free of charge only to Lebanese individuals
Syrian children aged between 0-18 years who were ad- infected with the virus. Syrian refugees are not includ-
mitted for reasons other than jaundice, to the outpa- ed in the LMoPH plan of free access to treatment. Data
tient infectious diseases clinics. Six of the 140 patients from the LMoPH-ESU [3] about the distribution of re-
(4.2%) were HBsAg positive, and all of these patients ported cases of HCV infection (Figure 3) reveals only few
were anti-HBc total positive and anti-HBs negative [13]. cases among Syrian refugees. This low incidence might
Anti-viral therapy for chronic HBV infection, when be due to the fact that they are not linked to medical
indicated, is provided free of charge to all Lebanese in- care following diagnosis and as such not reported the
dividuals who qualify for treatment. Non-lebanese in- LMoPH-ESU. This may allow the virus to circulate freely
cluding Syrian refugees residing in the country are not among refugees leading to fatal complications including
linked to any similar program of care. This may allow the advanced liver disease, hepatocellular carcinoma and
virus to circulate undetected among this group, making cirrhosis [17].

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Figure 3: The reported cases of HCV to LMoPH-ESU from 2008 till 2018 including Lebanese nationals and Syrian refugees.

Figure 4: The reported cases of Measles to LMoPH-ESU from 2008 till 2018 including Lebanese nationals and Syrian
refugees.

Measles representing 79 % of all cases. Most of the patients were

either not vaccinated or their vaccination status was
The annual number of reported cases of measles in-
not known [18]. The efficient transmissibility of measles
creased from only 9 cases in 2012 to 1760 in 2013 with
virus along with overpopulation and unsanitary condi-
82% being Lebanese and 13% Syrians [18] (Figure 4).
tions make the Syrian refugees highly susceptible to this
Those less than 10 years of age were mostly affected
infection [19]. Several vaccination campaigns were con-

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ducted to immunize both Lebanese and Syrian children. [18]. The LMoPH immunization schedule against the
In 2014, as part of the fourth national integrated immu- MMR was modified where the first dose is introduced
nization campaign, 1,165,871 children were vaccinated at 12 months of age and the second at 18 months. This
against measles and a steep decrease in the number variation from the USA schedule was mitigated by the
of cases was evident [18,19]. In 2014, UNICEF, in sup- recent measles outbreak of 2013 [14].
port of LMoPH, held a nationwide vaccination campaign Despite the high number of Syrians in Lebanon, the
and focused on routine immunization of lebanese and number of reported mumps cases was relatively low [18].
Syrian children. The number of reported measles cas- This may be explained by either the good coverage immu-
es dropped by the end of year 2016 to 44. However, nization rates in Syria before the crisis or due to the lack
the number of measles cases resurged again in 2018 of proper surveillance efforts by the Lebanese authorities
to reach 938 cases (Figure 4). The majority were either (Figure 5) [18]. In 2015, a surge in mumps cases was no-
unvaccinated or didn’t receive the second dose of the ticed reaching 1496. However, as of 2016, the number of
vaccine [20]. Measles reemergence is a good example reported cases was continuously dropping and this might
of the need to revisit immunization national policies in be contributed to the active MMR vaccination campaigns
view of the emerging migration. Outbreaks of measles carried out by the Lebanese health authorities targeting
have been documented in migrant populations in Eu- both lebanese and syrian children [20].
rope [21] and the International Organization for Migra-
tion (IOM) has recommended vaccination for recently Salmonella
arrived migrants/refugees [22]. A recent study showed Salmonellosis is endemic in Lebanon and risk of out-
a striking variation in policies on optimum approaches breaks is always present [24]. Prevalence increases with
to vaccination in migrants across Europe. There was a poor hygiene and underdeveloped public health infra-
call for more research and data collection, and need for structure [25]. Despite the large number of syrian ref-
dissemination of migrant-specific guidance [23]. ugees and the suboptimal health conditions, an annual
Mumps average of 26 cases of salmonella infection was report-
ed among this population between 2013 and 2016 as
In 2014 and 2015 there was a nation-wide out- compared to an annual average number of 495 cases
break of mumps when 1320 cases were reported to the among the lebanese citizens (Figure 6). This may re-
LMoPH-ESU (Figure 5). The majority of cases occurred in flect suboptimal surveillance and reporting efforts. Ac-
BeKaa, district close to the Syrian borders, where large cording to the CDC, it is estimated that for every one
number of Syrian refugees reside. This mumps outbreak laboratory confirmed case of salmonella, there are 29
occurred two years after the measles outbreak of 2013 unconfirmed cases [26]. In Jordan it is believed that for

Figure 5: The reported cases of Measles to LMoPH-ESU from 2008 till 2018 including Lebanese nationals and Syrian
refugees.

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Figure 6: The reported cases of Salmonella to LMoPH-ESU from 2008 till 2016 including Lebanese nationals and Syrian
refugees.

Figure 7: The reported cases of Brucella to LMoPH-ESU from 2008 till 2018 including Lebanese nationals and Syrian
refugees.

each laboratory confirmed salmonella infection there spread of salmonella among syrian refugees and host
are about 273 infected persons in the community [27]. community [12].
The number of reported cases in Lebanon among na-
tionals and syrians does not reflect the true incidence of
Brucellosis
the disease and more efforts are needed to monitor the Brucellosis is an endemic zoonotic disease in the

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DOI: 10.23937/2474-3658/1510172 ISSN: 2474-3658

Middle East region with Syria being the country with the year and prevalence is 20/100,000 [32]. Despite this
highest incidence in the world. Large numbers of animals positive note, Lebanon remains at risk of an increasing
are infected in Syria thereby causing significant human TB burden; the country is located in a conflict area and
disease [28]. Although brucellosis is endemic in Lebanon a constant recipient of large numbers of displaced peo-
and the occurrence of human disease is not uncommon ple. After a marked decrease in reported TB cases from
[29], the last few years have witnessed a progressive in- 663 in 1999 to 375 cases in 2006, the number rose again
crease in the incidence of reported human brucellosis reaching 689 in 2013, where the non-Lebanese consti-
cases (Figure 7) [18]. This increase might be attributed tuted the majority of cases 348/341 including 106 syrian
to high numbers of infected individuals among the Syr- refugees. In 2012, the Lebanese accounted for around
ian refugees and to the uncontrolled and illegal animal 52% of all reported cases of active TB cases with the
migration (live stocks and cattle) [30] between the two Ethiopians ranking second (28%) followed by Syrians
countries. The literature cites two cases of brucellosis (16%). In the past 5 years this case distribution is shifting
in Syrian refugees, one in Netherland and the other in towards more non-Lebanese being affected exceeding
Germany. The Netherland case was a 14-year-old boy 50% of total number of cases (Figure 8) [32]. The shift
who was diagnosed with neurobrucellosis, and brucel- in the incidence of active TB cases from Lebanese to
la melitensis was identified in the cerebrospinal fluid. non-Lebanese mainly Ethiopians and Syrians may result
The German case [31] was a teenage woman migrating in more individuals being affected and potential rise in
from syria. She became febrile postpartum and blood the number of multidrug resistance TB (MDR-TB) cases.
cultures revealed brucella melitensis.
The NTP has a treatment success rate reaching 90%
Tuberculosis (TB) among Lebanese nationals. However, the treatment
success rate remains below the desired levels among
Conflicts and crises during war time contribute to
the non-Lebanese patients [18,32].
migration and population displacements, and are often
associated with increases in the risk of TB reaching up Two basic strategies are critical to the prevention and
20-foldss [31]. The NTP estimates that the total annual control of TB. The first priority is identifying and treat-
number of reported cases of active TB ranges between ing all people who have active TB. The second is con-
500 and 700 cases, with a steep increase over the past tact screening and treating [34]. The Lebanese health
few years [32] (Figure 8). According to the WHO Global authorities provide adequate and free treatment to all
TB reports, country profile section, Lebanon is not con- TB cases residing in the country including Syrian refu-
sidered to be a high burden country regarding TB [33] gees [18,32,33,35]. Implementing this strategy to Syrian
where the estimated incidence rate is 16/100,000 per refugees faces several obstacles mainly due to security

Figure 8: Trend of TB cases notification in national and non-national population by years from 2008 until 2019 According
to NTP.

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Figure 9: The reported cases of leishmania to the LMoPH-ESU form 2008 till 2018 including Lebanese nationals and
Syrian refugees.

reasons, political affiliations and residence in difficult to and disseminating public awareness and health educa-
reach rural areas. This remains a major concern espe- tion material [37].
cially if we consider the MDR-TB strains scattered across
Similarly, in Turkey the open border policy of turk-
Syria reaching 62.5% [36]. In 2013, MDR-TB prevalence
ish government allowed for large number of displaced
was 3% among Syrians in Lebanon as compared to 5%
Syrians to live in camps and according to the reports of
in Jordan [37].
Turkish Disaster and Emergency Management Presiden-
Leishmaniasis cy, the number of registered refugees residing in camps
reached 22.088 in 2013 [41]. This resulted in emergence
An outbreak of leishmaniasis was reported among
of leishmaniasis which peaked in 2013 and gradually
Syrian refugees residing in Lebanon in early 2013 [18].
decreased to three cases by 2015, while the registered
Al Salem, et al. demonstrated that cutaneous leishman-
number of Syrian refugees increase to 38.293 in the
iasis prevalence corresponds with the presence of ref-
same year [40].
ugee camps [38]. According to the LMoPH-ESU data,
1033 cases were reported between 2013 and 2014, with Limitations
96.6% of those affected being Syrian refugees [18]. The
Data concerning syrians residing in Lebanon prior
dense concentration of Syrian refugees along with min-
to the crisis was not available at the LMPH-ESU. While
imal health care access in rural areas contributed to the
there is evidence of an increase in occurrence of sever-
increased incidences of leishmaniasis in Lebanon [19].
al infectious diseases after the syrian influx to Lebanon,
Risk factors for cutaneous leishmaniasis include poverty,
direct correlation cannot be established through the
malnourishment, population displacement, suppressed
available data. This report presents information main-
immunity, and poor housing [39]. Interventions by the
ly based on literature reviews and surveillance data
LMPH led to containment of the disease and significant
carried by LMPH-ESU, NTP and some actively involved
drop in leishmaniasis cases to 125, 110, 256, cases in
non-governmental organizations; hence, different col-
2015, 2017 and 2018 respectively, and near elimination
lection modalities, target population, sampling and se-
of the disease in 2018 (Figure 9) [40].
lection methods were accumulated. Therefore, direct
This drop in numbers of new cases is mainly attribut- comparisons and recommendations for preventative
ed to the WHO support to the LMPH in developing a measures cannot be definitive.
strategic response plan based on strengthening the
surveillance system, establishing an updated national Conclusion
treatment protocol, putting in place a referral system of The influx of Syrians seeking refuge in Lebanon is as-
twelve treatment clinics across Lebanon and producing sociated with multiple unwanted effects. The infectious

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DOI: 10.23937/2474-3658/1510172 ISSN: 2474-3658

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