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<article xmlns:xlink="http://www.w3.org/1999/xlink" article-type="research-article" dtd-version="2.0">
  <front>
    <journal-meta>
      <journal-id journal-id-type="publisher-id">JPH</journal-id>
      <journal-id journal-id-type="nlm-ta">JMIR Public Health Surveill</journal-id>
      <journal-title>JMIR Public Health and Surveillance</journal-title>
      <issn pub-type="epub">2369-2960</issn>
      <publisher>
        <publisher-name>JMIR Publications</publisher-name>
        <publisher-loc>Toronto, Canada</publisher-loc>
      </publisher>
    </journal-meta>
    <article-meta>
      <article-id pub-id-type="publisher-id">v6i1e14439</article-id>
      <article-id pub-id-type="pmid">32207696</article-id>
      <article-id pub-id-type="doi">10.2196/14439</article-id>
      <article-categories>
        <subj-group subj-group-type="heading">
          <subject>Original Paper</subject>
        </subj-group>
        <subj-group subj-group-type="article-type">
          <subject>Original Paper</subject>
        </subj-group>
      </article-categories>
      <title-group>
        <article-title>Trend of Cutaneous Leishmaniasis in Jordan From 2010 to 2016: Retrospective Study</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="editor">
          <name>
            <surname>Mohsni</surname>
            <given-names>Ezzeddine</given-names>
          </name>
        </contrib>
      </contrib-group>
      <contrib-group>
        <contrib contrib-type="reviewer">
          <name>
            <surname>Alyahya</surname>
            <given-names>Mohamamd</given-names>
          </name>
        </contrib>
        <contrib contrib-type="reviewer">
          <name>
            <surname>Khatatbeh</surname>
            <given-names>Moawiah</given-names>
          </name>
        </contrib>
      </contrib-group>
      <contrib-group>
        <contrib id="contrib1" contrib-type="author" corresp="yes">
          <name name-style="western">
            <surname>Alhawarat</surname>
            <given-names>Mohammad</given-names>
          </name>
          <degrees>MD</degrees>
          <xref rid="aff1" ref-type="aff">1</xref>
          <address>
            <institution>Jordan Field Epidemiology Training Program</institution>
            <institution>Jordan Ministry of Health</institution>
            <addr-line>Pr. Hamzah St</addr-line>
            <addr-line>Amman, 11118</addr-line>
            <country>Jordan</country>
            <phone>962 772300390</phone>
            <email>fazza200079@yahoo.com</email>
          </address>
          <ext-link ext-link-type="orcid">https://orcid.org/0000-0002-0133-6724</ext-link>
        </contrib>
        <contrib id="contrib2" contrib-type="author" equal-contrib="yes">
          <name name-style="western">
            <surname>Khader</surname>
            <given-names>Yousef</given-names>
          </name>
          <degrees>SCD</degrees>
          <xref rid="aff2" ref-type="aff">2</xref>
          <ext-link ext-link-type="orcid">https://orcid.org/0000-0002-7830-6857</ext-link>
        </contrib>
        <contrib id="contrib3" contrib-type="author">
          <name name-style="western">
            <surname>Shadfan</surname>
            <given-names>Bassam</given-names>
          </name>
          <degrees>MD</degrees>
          <xref rid="aff3" ref-type="aff">3</xref>
          <ext-link ext-link-type="orcid">https://orcid.org/0000-0001-9975-3691</ext-link>
        </contrib>
        <contrib id="contrib4" contrib-type="author">
          <name name-style="western">
            <surname>Kaplan</surname>
            <given-names>Nasser</given-names>
          </name>
          <degrees>PhD</degrees>
          <xref rid="aff2" ref-type="aff">2</xref>
          <ext-link ext-link-type="orcid">https://orcid.org/0000-0003-0561-1794</ext-link>
        </contrib>
        <contrib id="contrib5" contrib-type="author">
          <name name-style="western">
            <surname>Iblan</surname>
            <given-names>Ibrahim</given-names>
          </name>
          <degrees>MD</degrees>
          <xref rid="aff1" ref-type="aff">1</xref>
          <ext-link ext-link-type="orcid">https://orcid.org/0000-0001-8538-977X</ext-link>
        </contrib>
      </contrib-group>
      <aff id="aff1">
        <label>1</label>
        <institution>Jordan Field Epidemiology Training Program</institution>
        <institution>Jordan Ministry of Health</institution>
        <addr-line>Amman</addr-line>
        <country>Jordan</country>
      </aff>
      <aff id="aff2">
        <label>2</label>
        <institution>Jordan University of Science and Technology</institution>
        <addr-line>Irbid</addr-line>
        <country>Jordan</country>
      </aff>
      <aff id="aff3">
        <label>3</label>
        <institution>Parasitic and Zoonotic Disease Department</institution>
        <institution>Communicable Disease Directorate</institution>
        <institution>Ministry of Health</institution>
        <addr-line>Amman</addr-line>
        <country>Jordan</country>
      </aff>
      <author-notes>
        <corresp>Corresponding Author: Mohammad Alhawarat <email>fazza200079@yahoo.com</email></corresp>
      </author-notes>
      <pub-date pub-type="collection">
        <season>Jan-Mar</season>
        <year>2020</year>
      </pub-date>
      <pub-date pub-type="epub">
        <day>24</day>
        <month>3</month>
        <year>2020</year>
      </pub-date>
      <volume>6</volume>
      <issue>1</issue>
      <elocation-id>e14439</elocation-id>
      <history>
        <date date-type="received">
          <day>18</day>
          <month>4</month>
          <year>2019</year>
        </date>
        <date date-type="rev-request">
          <day>30</day>
          <month>5</month>
          <year>2019</year>
        </date>
        <date date-type="rev-recd">
          <day>4</day>
          <month>10</month>
          <year>2019</year>
        </date>
        <date date-type="accepted">
          <day>20</day>
          <month>10</month>
          <year>2019</year>
        </date>
      </history>
      <copyright-statement>©Mohammad Alhawarat, Yousef Khader, Bassam Shadfan, Nasser Kaplan, Ibrahim Iblan. Originally published in JMIR Public Health and Surveillance (http://publichealth.jmir.org), 24.03.2020.</copyright-statement>
      <copyright-year>2020</copyright-year>
      <license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/">
        <p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work, first published in JMIR Public Health and Surveillance, is properly cited. The complete bibliographic information, a link to the original publication on http://publichealth.jmir.org, as well as this copyright and license information must be included.</p>
      </license>
      <self-uri xlink:href="http://publichealth.jmir.org/2020/1/e14439/" xlink:type="simple"/>
      <abstract>
        <sec sec-type="background">
          <title>Background</title>
          <p>Cutaneous leishmaniasis (CL) is endemic in the Middle East, with countries such as Syria reporting high incidence rates.</p>
        </sec>
        <sec sec-type="objective">
          <title>Objective</title>
          <p>This study aimed to assess the trends in the incidence of cutaneous leishmaniasis (CL) in Jordan from 2010 to 2016.</p>
        </sec>
        <sec sec-type="methods">
          <title>Methods</title>
          <p>This retrospective study included all cases of CL that had been reported to the Leishmaniasis Surveillance System in the Department of Communicable Diseases at the Jordan Ministry of Health during the period from 2010 to 2016. A total of 1243 cases were reported and met the case definition.</p>
        </sec>
        <sec sec-type="results">
          <title>Results</title>
          <p>A total of 1243 cases (60.65% [754/1243] males and 39.34% [489/1243] females) were diagnosed during the study period. Of this sample, 233 patients (19.13%) were aged &#60;5 years old, 451 (37.03%) were aged between 5-14 years old, 190 (15.60%) were aged between 15-24 years old, and 344 (28.24%) were aged ≥25 years old. Of those, 646 (51.97%) were Jordanians and 559 (44.97%) were Syrians. The average annual incidence rate of 1.70 per 100,000 people between 2010 and 2013 increased to 3.00 per 100,000 people in the years 2014 to 2016. There was no difference in incidence rates between Jordanians and Syrian refugees between 2010 and 2012. After 2012, the incidence rate increased significantly among Syrian refugees from 1.20 per 100,000 people in 2012 to 11.80 per 100,000 people in 2016. On the contrary, the incidence rate did not change significantly among Jordanians.</p>
        </sec>
        <sec sec-type="conclusions">
          <title>Conclusions</title>
          <p>The incidence rate of leishmaniasis in Jordan has increased in the last three years because of the influx of Syrian refugees into Jordan. A massive effort toward reservoir and vector control, along with actively pursuing diagnosis in endemic foci, will be helpful. Proper and studious reporting of cases is also a necessity for the eradication of this disease.</p>
        </sec>
      </abstract>
      <kwd-group>
        <kwd>cutaneous leishmaniasis</kwd>
        <kwd>incidence</kwd>
        <kwd>Jordan</kwd>
      </kwd-group>
    </article-meta>
  </front>
  <body>
    <sec sec-type="introduction">
      <title>Introduction</title>
      <sec>
        <title>Background</title>
        <p>Leishmaniasis is a vector-borne disease that is transmitted via female sandflies and caused by an intracellular protozoon called Leishmania. It is endemic in 98 countries and 3 continents [<xref ref-type="bibr" rid="ref1">1</xref>]. Out of 30 mammal-infecting Leishmania species, 21 are known to infect humans [<xref ref-type="bibr" rid="ref1">1</xref>]. Leishmaniasis is subdivided into 3 types: cutaneous, mucocutaneus, and visceral. Cutaneous leishmaniasis (CL) is the most common type, and almost 95% of its cases are found in North and South America, the Mediterranean region, the Middle East, and Central Asia [<xref ref-type="bibr" rid="ref2">2</xref>]. It usually manifests in the form of skin lesions, particularly ulcers, which leave permanent scars and cause severe disability. An estimate of around 0.7 to 1.3 million new cases are reported each year, and more than two-thirds of the new cases are found in 6 countries: Afghanistan, Algeria, Brazil, Colombia, Iran, and Syria [<xref ref-type="bibr" rid="ref2">2</xref>].</p>
        <p>Poverty, overcrowding, immigration, and other risk factors have a great role in increasing the incidence of CL. There are currently no available drugs or vaccines to prevent infections, and despite numerous preventative measures, leishmaniasis remains an important, neglected, zoonotic disease and a big challenge to public health, especially in underdeveloped countries [<xref ref-type="bibr" rid="ref3">3</xref>]. The trends of CL vary from one country to another in the Middle East. The incidence rate has decreased in Saudi Arabia, whereas it has increased in Iraq and Syria, especially during the civil war [<xref ref-type="bibr" rid="ref4">4</xref>]. In general, previous studies in the Middle East have shown that males are more likely to be affected with CL [<xref ref-type="bibr" rid="ref5">5</xref>-<xref ref-type="bibr" rid="ref7">7</xref>].</p>
        <p>In Jordan, it has been an emerging disease since the 1980s, and is still an important public health problem despite existing control and prevention measures. In a previous study in the last decades, the incidence rate of CL in Jordan has been shown to be increasing [<xref ref-type="bibr" rid="ref8">8</xref>]. One study had assessed the spatial and temporal characteristics of CL in the years from 1999 to 2010, pre–Arab Spring in Jordan and Syria, and it showed that the risk of CL varied both spatially and temporally in both countries [<xref ref-type="bibr" rid="ref9">9</xref>]. That study showed that the patterns of the disease in Jordan could be described as relatively low and heterogeneous whereas those in Syria were relatively much higher and less heterogeneous.</p>
      </sec>
      <sec>
        <title>Objectives</title>
        <p>The CL surveillance system in Jordan receives reports on a weekly basis from 21 reporting sites from all districts and governorates in the country. This study aimed to assess the trend in the incidence of CL in Jordan from 2010 to 2016.</p>
      </sec>
    </sec>
    <sec sec-type="methods">
      <title>Methods</title>
      <p>This retrospective study included all cases of CL that had been reported to the Leishmaniasis Surveillance System in the Department of Communicable Diseases at the Jordan Ministry of Health during the period from 2010 to 2016. A total of 1243 cases were reported and met the case definition.</p>
      <p>A suspected case is defined as a person who was in Jordan during the study period and showed clinical signs (skin lesions) of infection, wherein the papule appears and may enlarge to become an indolent ulcerated nodule. A confirmed case is a person who was in Jordan during the study period and showing clinical signs of infection, with paracytological confirmation of the diagnosis by a positive smear or culture from a skin lesion [<xref ref-type="bibr" rid="ref10">10</xref>].</p>
      <p>The necessary and available data were retrieved from the surveillance system. Data included patient’s age, gender, address, nationality, occupation, reporting site, reporting month, reporting year, and location of lesion. The Ethical Committee at the Ministry of Health approved the study. Data were entered into an Excel (Microsoft, Redmond, Washington, United States) file and analyzed using SPSS Statistics for Windows, Version 23.0 (IBM Corporation, Armonk, New York, United States).</p>
    </sec>
    <sec sec-type="results">
      <title>Results</title>
      <sec>
        <title>Patients’ Characteristics</title>
        <p>A total of 1243 CL cases were reported. Of the total reported cases, 754 (60.65%) were males, 489 (39.34%) were females, and the mean age of the patients was 18.6 years old (SD 16.8). Overall, 233 (19.13%) patients were aged &#60;5 years old, 451 (37.03%) were aged between 5-14 years old, 190 (15.60%) were aged between 15-24 years old, and 344 (28.24%) were aged ≥25 years old. Half of reported cases were from the southern region of the country (<xref ref-type="table" rid="table1">Table 1</xref>). A total 563 (45.29%) patients had head lesions, 186 (14.96%) had trunk lesions, 382 (381.60%) had leg lesions, and 426 (34.27%) had arm lesions.</p>
        <table-wrap position="float" id="table1">
          <label>Table 1</label>
          <caption>
            <p>Distribution of leishmaniasis cases in Jordan from 2010 to 2016 by age, gender, and region.</p>
          </caption>
          <table width="1000" cellpadding="5" cellspacing="0" border="1" rules="groups" frame="hsides">
            <col width="30"/>
            <col width="400"/>
            <col width="570"/>
            <thead>
              <tr valign="top">
                <td colspan="2">Characteristics</td>
                <td>Frequency, n (%)</td>
              </tr>
            </thead>
            <tbody>
              <tr valign="top">
                <td colspan="2">
                  <bold>Age (years)</bold>
                </td>
                <td>
                  <break/>
                </td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>0-4</td>
                <td>233 (19.1)</td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>5-14</td>
                <td>451 (37.0)</td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>15-24</td>
                <td>190 (15.6)</td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>≥25</td>
                <td>344 (28.2)</td>
              </tr>
              <tr valign="top">
                <td colspan="2">
                  <bold>Gender</bold>
                </td>
                <td>
                  <break/>
                </td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>Male</td>
                <td>754 (60.7)</td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>Female</td>
                <td>489 (39.3)</td>
              </tr>
              <tr valign="top">
                <td colspan="2">
                  <bold>Region</bold>
                </td>
                <td>
                  <break/>
                </td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>South</td>
                <td>575 (49.4)</td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>North</td>
                <td>179 (15.4)</td>
              </tr>
              <tr valign="top">
                <td>
                  <break/>
                </td>
                <td>Middle</td>
                <td>410 (35.2)</td>
              </tr>
            </tbody>
          </table>
        </table-wrap>
      </sec>
      <sec>
        <title>Incidence and Trend</title>
        <p>The average annual incidence rate was 1.70% among 100,000 people during the period from 2010 to 2013. In the period from 2014 to 2016, when Syrian refugees entered the country, the average incidence rate increased to 3.00% in every 100,000 people (<xref rid="figure1" ref-type="fig">Figure 1</xref>). The incidence rate was higher among those aged less than 15 years old compared with those aged ≥15 years old (<xref rid="figure2" ref-type="fig">Figure 2</xref>), and it was higher among males compared to females in all studied years. In both genders, the incidence decreased during the period from 2010 to 2012, following which it started to increase again (<xref rid="figure3" ref-type="fig">Figure 3</xref>). In total, 646 (51.97%) of reported leishmaniasis cases were Jordanians and 559 (44.97%) were Syrians. There was no difference in incidence rates between Jordanian and Syrian refugees between 2010 and 2012, but after 2012, the incidence rate increased significantly among Syrian refugees from 1.20 per 100,000 people in 2012 to 11.80 per 100,000 people in 2016. On the contrary, the incidence rate did not change significantly among Jordanians (<xref rid="figure4" ref-type="fig">Figure 4</xref>).</p>
        <fig id="figure1" position="float">
          <label>Figure 1</label>
          <caption>
            <p>The trend of the overall incidence rate of cutaneous leishmaniasis per 100,000 people in Jordan from 2010 to 2016.</p>
          </caption>
          <graphic xlink:href="publichealth_v6i1e14439_fig1.png" alt-version="no" mimetype="image" position="float" xlink:type="simple"/>
        </fig>
        <fig id="figure2" position="float">
          <label>Figure 2</label>
          <caption>
            <p>The incidence rate of cutaneous leishmaniasis per 100,000 people in Jordan by age categories from 2010 to 2016.</p>
          </caption>
          <graphic xlink:href="publichealth_v6i1e14439_fig2.png" alt-version="no" mimetype="image" position="float" xlink:type="simple"/>
        </fig>
        <fig id="figure3" position="float">
          <label>Figure 3</label>
          <caption>
            <p>The incidence rate of cutaneous leishmaniasis per 100,000 people in Jordan by gender from 2010 to 2016.</p>
          </caption>
          <graphic xlink:href="publichealth_v6i1e14439_fig3.png" alt-version="no" mimetype="image" position="float" xlink:type="simple"/>
        </fig>
        <fig id="figure4" position="float">
          <label>Figure 4</label>
          <caption>
            <p>The incidence rate of cutaneous leishmaniasis per 100,000 people in Jordan by nationality from 2010 to 2016.</p>
          </caption>
          <graphic xlink:href="publichealth_v6i1e14439_fig4.png" alt-version="no" mimetype="image" position="float" xlink:type="simple"/>
        </fig>
      </sec>
    </sec>
    <sec sec-type="discussion">
      <title>Discussion</title>
      <sec>
        <title>Principal Findings</title>
        <p>This study assessed changes in the incidence of CL in Jordan between 2010 and 2016. Males were predominant among affected cases in all age categories, and this finding was also reported in other countries, including Saudi Arabia and Iran [<xref ref-type="bibr" rid="ref5">5</xref>-<xref ref-type="bibr" rid="ref7">7</xref>]. The increased infection rates among males in Jordan might be explained by the fact that males are usually responsible for outdoor work and work in farms. Moreover, most females in Jordan traditionally cover most parts of their bodies, thus they are fairly well protected from sandflies.</p>
        <p>During the study period, the highest incidence rate was among subjects aged less than 15 years old. This finding is consistent with the findings from a longitudinal study in the endemic area in the eastern region of Saudi Arabia [<xref ref-type="bibr" rid="ref11">11</xref>], and with the findings of other studies in Saudi Arabia and Iran [<xref ref-type="bibr" rid="ref5">5</xref>-<xref ref-type="bibr" rid="ref7">7</xref>]. This finding is probably explained by the fact that children spend more time outdoors, and therefore are more likely to be exposed to sandfly bites. However, other studies in Saudi Arabia [<xref ref-type="bibr" rid="ref12">12</xref>], Iran [<xref ref-type="bibr" rid="ref13">13</xref>], and Kuwait [<xref ref-type="bibr" rid="ref14">14</xref>] have shown that people aged between 21-30 years old are the most susceptible because most laborers are in this age group.</p>
        <p>On the basis of the geographic distribution of CL, the southern region of Jordan was an endemic area. However, the Zarqa governorate is now a new hot reporting site because of the presence of the Syrian refugees’ camp in this governorate. In agreement with the findings of studies in Lebanon [<xref ref-type="bibr" rid="ref15">15</xref>] and Turkey [<xref ref-type="bibr" rid="ref16">16</xref>], this study showed an increasing trend in the incidence rate of CL in Jordan during the study period. The increased rate of CL in Jordan in the past few years is explained by an increasing number of Syrian refugees in Jordan over time. Poor housing, absence of clean water, inadequate sanitation, deficient medical facilities and services, and abundant sandfly populations have contributed to CL among Syrian refugees.</p>
        <p>CL emerged in areas where displaced Syrians and disease reservoirs coexist. In 2013, 1033 new cases were reported in Lebanon, of which 96.6% occurred among the displaced Syrian refugee populations [<xref ref-type="bibr" rid="ref15">15</xref>]. In Turkey, nonendemic parasite strains (<italic>Leishmania major</italic> and <italic>Leishmania donovani</italic>) were introduced by incoming refugees [<xref ref-type="bibr" rid="ref16">16</xref>]. Other studies in Saudi Arabia and Iran have shown a decline in the number and incidence rate of CL in the same period [<xref ref-type="bibr" rid="ref5">5</xref>,<xref ref-type="bibr" rid="ref6">6</xref>]. The main limitation of this study is the underreporting of CL cases.</p>
      </sec>
      <sec>
        <title>Conclusions</title>
        <p>In conclusion, CL is increasing in Jordan, especially after the Syrian war, but countries with ample resources, like Jordan, have taken measures to control the spread of the disease. However, challenges still remain to be solved because of huge refugee movement into the country. A massive effort toward reservoir and vector control, along with actively pursuing diagnosis in endemic foci, will be helpful. Proper and studious reporting of cases is also a necessity for the eradication of this disease, as health care practitioners rely on these data for framing health policies. Future research is needed to determine the main risk factors contributing to the increasing trend of the occurrence of leishmaniasis, and to implement and evaluate control and prevention measures in Jordan. Moreover, there is an urgent need for developing national health policies and action plans for combating CL in Jordan.</p>
      </sec>
    </sec>
  </body>
  <back>
    <app-group/>
    <glossary>
      <title>Abbreviations</title>
      <def-list>
        <def-item>
          <term id="abb1">CL</term>
          <def>
            <p>cutaneous leishmaniasis</p>
          </def>
        </def-item>
      </def-list>
    </glossary>
    <ack>
      <p>The authors would like to acknowledge the Eastern Mediterranean Public Health Network and Jordan Field Epidemiology Training Program for their technical support.</p>
    </ack>
    <fn-group>
      <fn fn-type="conflict">
        <p>None declared.</p>
      </fn>
    </fn-group>
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