<?xml version="1.0" encoding="UTF-8"?><!DOCTYPE article  PUBLIC "-//NLM//DTD Journal Publishing DTD v3.0 20080202//EN" "http://dtd.nlm.nih.gov/publishing/3.0/journalpublishing3.dtd"><article xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" dtd-version="3.0" xml:lang="en" article-type="research article"><front><journal-meta><journal-id journal-id-type="publisher-id">OJPed</journal-id><journal-title-group><journal-title>Open Journal of Pediatrics</journal-title></journal-title-group><issn pub-type="epub">2160-8741</issn><publisher><publisher-name>Scientific Research Publishing</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="doi">10.4236/ojped.2021.112029</article-id><article-id pub-id-type="publisher-id">OJPed-110185</article-id><article-categories><subj-group subj-group-type="heading"><subject>Articles</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine&amp;Healthcare</subject></subj-group></article-categories><title-group><article-title>
 
 
  Prevalence of Soil-Transmitted Helminths and Intestinal Protozoa among School Children in Lome, Togo
 
</article-title></title-group><contrib-group><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Monique</surname><given-names>A. Dorkenoo</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Foli</surname><given-names>Agbeko</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Harishu</surname><given-names>Dokoto</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Dave</surname><given-names>Plate</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Mawouto</surname><given-names>Fiawoo</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Kossi</surname><given-names>Yakpa</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Efoe</surname><given-names>Sossou</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Sevi</surname><given-names>K. Sognikin</given-names></name><xref ref-type="aff" rid="aff7"><sup>7</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Adama</surname><given-names>Dodji Gbadoe</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author" xlink:type="simple"><name name-style="western"><surname>Rachel</surname><given-names>Bronzan</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib></contrib-group><aff id="aff7"><addr-line>Programme National de Lutte Intégrée contre les Maladies Tropicales Négligées, Ministère de la Santé et de l’Hygiène Publique, Lomé, Togo</addr-line></aff><aff id="aff6"><addr-line>Division des Laboratoires, Ministère de la Santé et de l’Hygiène Publique, Lomé, Togo</addr-line></aff><aff id="aff2"><addr-line>Département de la Pédiatrie, Centre Hospitalier Universitaire Campus, Lomé, Togo</addr-line></aff><aff id="aff3"><addr-line>H&amp;amp;ocirc;pital d’Instruction des Armées, Centre Universitaire de Cotonou, Cotonou, Benin</addr-line></aff><aff id="aff5"><addr-line>Département de la Pédiatrie, Faculté des Sciences de la santé, Université de Lomé, Lomé, Togo</addr-line></aff><aff id="aff4"><addr-line>Hope Education Foundation, Pompano, Florida, USA</addr-line></aff><aff id="aff1"><addr-line>Département des Sciences Fondamentales et Biologiques, Faculté des Sciences de la santé, Université de Lomé, Lomé, Togo</addr-line></aff><aff id="aff8"><addr-line>Health and Development International, Newburyport, USA</addr-line></aff><pub-date pub-type="epub"><day>28</day><month>04</month><year>2021</year></pub-date><volume>11</volume><issue>02</issue><fpage>313</fpage><lpage>328</lpage><history><date date-type="received"><day>13,</day>	<month>April</month>	<year>2021</year></date><date date-type="rev-recd"><day>26,</day>	<month>June</month>	<year>2021</year>	</date><date date-type="accepted"><day>29,</day>	<month>June</month>	<year>2021</year></date></history><permissions><copyright-statement>&#169; Copyright  2014 by authors and Scientific Research Publishing Inc. </copyright-statement><copyright-year>2014</copyright-year><license><license-p>This work is licensed under the Creative Commons Attribution International License (CC BY). http://creativecommons.org/licenses/by/4.0/</license-p></license></permissions><abstract><p>
 
 
  Background:
   Significant morbidity in children is associated with infectio
  us
   diseases especially soil-transmitted helminth (STH) infections which are prevalent in sub
  -
  Saharan African countries. The objective of this study is to estimate the prevalence of STH and intestinal protozoa among schoolchildren in Lom&#233;, Togo. <b>Patients and Methods:</b> In November 2013, in each of the five districts of the Lom&#233;-commune region, thirty pupils per level of the third, fourth, fifth and sixth grades of five primary schools were included. Each child submitted a single stool sample that was analyzed by the Kato-Katz method for STH. In addition, stool
   
  samples of school children selected in third and sixth grades were examined by direct visualization using saline and Lugol’s stain for intestinal protozoa. <b>Results:</b> A total of 2944 children were enrolled at 25 schools. The overall prevalence of STH at schools was 5.0% (range 1.5% to 8.6%), was higher in boys than girls, and increased with age and grade. Hookworm was the most prevalent species (3.4% of children surveyed). Intestinal protozoa were found in 52.2% (765/1465) of children tested and commensal amoebae represented 22.7% of these protozoa identified. Entamoeba histolytica/dispar/moshkovskii and Giardia intestinalis were identified in 2.3% and 11.5% of children, respectively. Co-infestation was noted in 1.35% of children with intestinal helminths and 12.2% of children with protozoa. <b>Conclusion:</b> Although a high prevalence of intestinal protozoa was found in our study, the majority were non-pathogenic protozoa and the low prevalence of STH among school-age children in Lom&#233;-commune region confirms that mass drug administration (MDA) is not needed. Children should receive additional education on best hygiene practices.
 
</p></abstract><kwd-group><kwd>Soil Transmitted Helminth</kwd><kwd> Intestinal Protozoa</kwd><kwd> Prevalence</kwd><kwd> Schoolchildren</kwd><kwd> Togo</kwd></kwd-group></article-meta></front><body><sec id="s1"><title>1. Introduction</title><p>Soil-transmitted helminth (STH) infections and other parasitic diseases are prevalent in the world, particularly in sub-Saharan Africa. In 2017, the number of people infected in the world was estimated at 1.2 billion, with 90% of infections occurring in sub-Saharan Africa [<xref ref-type="bibr" rid="scirp.110185-ref1">1</xref>]. These parasites are often associated with stunted growth, micronutrient deficiency leading to decreased resistance to infection, cognitive impairment, educational difficulties among children and, later, low social and economic productivity [<xref ref-type="bibr" rid="scirp.110185-ref2">2</xref>]. Hookworm also causes anemia and increases maternal morbidity and low birth weight, thus maintaining a vicious cycle of morbidity and poverty [<xref ref-type="bibr" rid="scirp.110185-ref3">3</xref>]. School-age children (SAC) are the population most at risk, but they also contribute significantly to transmission. A key strategy recommended by WHO against these infections is morbidity control through mass drug administration (MDA) of preventive chemotherapy (PC) with albendazole or mebendazole targeting high-risk groups such as pre-school and school-age children, women of childbearing age and, since 2013, any adult at high risk [<xref ref-type="bibr" rid="scirp.110185-ref4">4</xref>]. PC should be conducted once per year if the prevalence in an ecological zone is between 20% and 49%, twice per year if it is 50% or higher, and individualized in communities with a prevalence of less than 20% [<xref ref-type="bibr" rid="scirp.110185-ref4">4</xref>]. In Togo, a national baseline survey conducted in 2009 found a high prevalence of STH [<xref ref-type="bibr" rid="scirp.110185-ref5">5</xref>] and in 2010, MDA with albendazole targeting SAC was initiated in areas where STH prevalence was 20% or more. During this baseline survey, the health region of Lom&#233;-commune, considered at low risk regarding the urban setting, was not evaluated. However, urban areas with high STH prevalence have been noted in the literature [<xref ref-type="bibr" rid="scirp.110185-ref6">6</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref7">7</xref>]. Since reliable current data were not available for this region with 1/7 of the entire population of Togo, field surveys to determine the disease prevalence within Lom&#233;-commune were needed. This evaluation was carried out in order to assess the need for albendazole MDA in this region [<xref ref-type="bibr" rid="scirp.110185-ref8">8</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref9">9</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref10">10</xref>]. The objectives of this study were to determine the prevalence of Ancylostoma duodenale, Necator americanus, Ascaris lumbricoides and Trichiuris trichiura and the prevalence of intestinal protozoa among schoolchildren.</p></sec><sec id="s2"><title>2. Patients and Method</title><p>This was a cross-sectional, school-based survey carried out from November 4 to 25, 2013 in the five districts of Lom&#233;-commune health region that together comprise the capital of Togo [<xref ref-type="bibr" rid="scirp.110185-ref11">11</xref>]. Located in the southern part of the country, Lom&#233; covers an area of 90.59 Km<sup>2</sup> with an estimated population of 1,018,840 inhabitants in 2018 out of a total population of 7,440,366 in Togo. The study enrolled pupils attending public primary schools in this region. For the school’s selection, all of the five health districts of Lom&#233;-Commune health region considered to be an ecological different entity, were selected. In each district, based on the following criteria, the area considered to be at high risk was chosen by mutual agreement with the district chief medical officers and the sanitation department of the Ministry of Health. These criteria are: 1) low drinking water coverage, 2) poor solid waste management, 3) poor wastewater management, and 4) low latrine coverage. High-risk areas were identified, and five schools were randomly selected in these areas in each of the five districts.</p><p>In each school, 30 students from each grade from third to sixth grade were surveyed. For each of the four classes, , the first children who presented a written parental consent form signed and who could provide a stool sample were enrolled until 30 children from the grade had been recruited. At each school, children from the equivalent of third fourth, fifth and sixth grade were enrolled. The day before the survey, a consent form was sent home to each child’s parent or guardian. On the day of the study, the first 30 children in each of the four grades who had received written parental consent, who declared they had not received any anti-helminthic drugs during the month prior the study, and who were able to provide a stool sample, were surveyed. Before stool collection, a questionnaire was used to record socio-demographic information. Stool testing for STH was performed using the Kato-Katz method; one slide per child was prepared and read by a laboratory technician using standard procedures and number of eggs per gram of stool was calculated for Ascaris lumbricoides, Trichuris trichiura, and hookworm. In addition, stools samples of pupils from third and sixth grade were examined by direct microscopy and with Lugol stain for intestinal protozoa.</p><p>Data were entered into CSPro and analyzed with Microsoft Excel 2007 and SPSS (Statistical Package for the Social Sciences). The prevalence of each intestinal parasite was estimated and, for STH, the intensity of infection was estimated based on the number of eggs median per gram (epg) of stool, according to the WHO classification [<xref ref-type="bibr" rid="scirp.110185-ref12">12</xref>]. Pearson’s Chi-square test and Fisher’s exact test (in cases where the expected values are less than 5) were used to compare the prevalence. The significance threshold for all statistical tests was set at α = 0.05.</p><p>The study protocol was reviewed and approved by the Bioethics Committee for Health Research of the Togo Ministry of Health. In addition, a signed written informed consent was obtained from the parents or guardian of each pupil enrolled in the study.</p><p>Any child who tested positive for at least one STH was treated free of charge with albendazole; those who tested positive for pathogenic intestinal protozoa received a prescription for the appropriate treatment.</p></sec><sec id="s3"><title>3. Results</title><sec id="s3_1"><title>3.1. Characteristics of the Study Population</title><p>A total of 2944 students in 25 schools in the 5 districts in Lom&#233;-commune region were enrolled. The mean age was 11 old years with a range from 7 to 16 years. Characteristics of the surveyed population are shown in <xref ref-type="table" rid="table1">Table 1</xref>.</p></sec><sec id="s3_2"><title>3.2. Prevalence of STH</title><p>Overall, 5.0% (148/2944) children tested positive for at least one STH. The prevalence of STH varied significatively across the five districts, from 1.5% in District N˚1 to 8.6% in District N˚2 (p &lt; 0.0001) (<xref ref-type="fig" rid="fig1">Figure 1</xref>).</p><p>Prevalence increased significantly with age; the highest prevalence was found in children over 15 years of age, 15.6% (p = 0.0001) (<xref ref-type="table" rid="table2">Table 2</xref>). Infection was significantly more prevalent in boys than girls (5.7% vs. 4.4%; p = 0.049). Hookworm was the predominant STH infection with a prevalence of 3.4%. A. lumbricoides and T. trichiura were each found in 0.8% of cases.</p><table-wrap id="table1" ><label><xref ref-type="table" rid="table1">Table 1</xref></label><caption><title> Socio-demographic characteristics of the study population</title></caption><table><tbody><thead><tr><th align="center" valign="middle" ></th><th align="center" valign="middle" ></th><th align="center" valign="middle" >District 1</th><th align="center" valign="middle" >District 2</th><th align="center" valign="middle" >District 3</th><th align="center" valign="middle" >District 4</th><th align="center" valign="middle" >District 5</th><th align="center" valign="middle" >Total</th></tr></thead><tr><td align="center" valign="middle" ></td><td align="center" valign="middle" ></td><td align="center" valign="middle" >n (%)</td><td align="center" valign="middle" >n (%)</td><td align="center" valign="middle" >n (%)</td><td align="center" valign="middle" >n (%)</td><td align="center" valign="middle" >n (%)</td><td align="center" valign="middle" >N (%)</td></tr><tr><td align="center" valign="middle"  rowspan="3"  >7 - 9 years</td><td align="center" valign="middle" >B</td><td align="center" valign="middle" >65 (2.2)</td><td align="center" valign="middle" >81 (2.7)</td><td align="center" valign="middle" >85 (2.9)</td><td align="center" valign="middle" >74 (2.5)</td><td align="center" valign="middle" >89 (3.0)</td><td align="center" valign="middle" >394 (13.4)</td></tr><tr><td align="center" valign="middle" >G</td><td align="center" valign="middle" >71 (2.4)</td><td align="center" valign="middle" >61 (2.1)</td><td align="center" valign="middle" >99 (3.4)</td><td align="center" valign="middle" >86 (2.9)</td><td align="center" valign="middle" >114 (3.9)</td><td align="center" valign="middle" >431 (14.6)</td></tr><tr><td align="center" valign="middle" >T</td><td align="center" valign="middle" >136 (4.6)</td><td align="center" valign="middle" >142 (4.8)</td><td align="center" valign="middle" >184 (6.3)</td><td align="center" valign="middle" >160 (5.4)</td><td align="center" valign="middle" >203 (6.9)</td><td align="center" valign="middle" >825 (28.0)</td></tr><tr><td align="center" valign="middle"  rowspan="3"  >10 - 12 years</td><td align="center" valign="middle" >B</td><td align="center" valign="middle" >102 (3.5)</td><td align="center" valign="middle" >180 (6.1)</td><td align="center" valign="middle" >131 (4.4)</td><td align="center" valign="middle" >135 (4.6)</td><td align="center" valign="middle" >158 (5.4)</td><td align="center" valign="middle" >706 (24.0)</td></tr><tr><td align="center" valign="middle" >G</td><td align="center" valign="middle" >113 (3.8)</td><td align="center" valign="middle" >145 (4.9)</td><td align="center" valign="middle" >174 (5.9)</td><td align="center" valign="middle" >175 (5.9)</td><td align="center" valign="middle" >193 (6.5)</td><td align="center" valign="middle" >800 (27.2)</td></tr><tr><td align="center" valign="middle" >T</td><td align="center" valign="middle" >215 (7.3)</td><td align="center" valign="middle" >325 (11.0)</td><td align="center" valign="middle" >305 (10.3)</td><td align="center" valign="middle" >310 (10.5)</td><td align="center" valign="middle" >351 (11.9)</td><td align="center" valign="middle" >1506 (51.2)</td></tr><tr><td align="center" valign="middle"  rowspan="3"  >13 - 15 years</td><td align="center" valign="middle" >B</td><td align="center" valign="middle" >51 (1.7)</td><td align="center" valign="middle" >57 (1.9)</td><td align="center" valign="middle" >45 (1.5)</td><td align="center" valign="middle" >59 (2.0)</td><td align="center" valign="middle" >59 (2.0)</td><td align="center" valign="middle" >271 (9.2)</td></tr><tr><td align="center" valign="middle" >G</td><td align="center" valign="middle" >56 (1.9)</td><td align="center" valign="middle" >61 (2.1)</td><td align="center" valign="middle" >51 (1.7)</td><td align="center" valign="middle" >66 (2.2)</td><td align="center" valign="middle" >82 (2.8)</td><td align="center" valign="middle" >316 (10.7)</td></tr><tr><td align="center" valign="middle" >T</td><td align="center" valign="middle" >107 (3.6)</td><td align="center" valign="middle" >118 (4.0)</td><td align="center" valign="middle" >96 (3.2)</td><td align="center" valign="middle" >125 (4.2)</td><td align="center" valign="middle" >141 (4.8)</td><td align="center" valign="middle" >587 (19.9)</td></tr><tr><td align="center" valign="middle"  rowspan="3"  >&gt;15 years</td><td align="center" valign="middle" >B</td><td align="center" valign="middle" >2 (0.1)</td><td align="center" valign="middle" >5 (0.2)</td><td align="center" valign="middle" >6 (0.2)</td><td align="center" valign="middle" >1 (0.0)</td><td align="center" valign="middle" >2 (0.1)</td><td align="center" valign="middle" >16 (0.5)</td></tr><tr><td align="center" valign="middle" >G</td><td align="center" valign="middle" >4 (0.1)</td><td align="center" valign="middle" >3 (0.1)</td><td align="center" valign="middle" >1 (0.0)</td><td align="center" valign="middle" >0 (0.0)</td><td align="center" valign="middle" >2 (0.1)</td><td align="center" valign="middle" >10 (0.3)</td></tr><tr><td align="center" valign="middle" >T</td><td align="center" valign="middle" >6 (0.2)</td><td align="center" valign="middle" >8 (0.3)</td><td align="center" valign="middle" >7 (0.2)</td><td align="center" valign="middle" >1 (0.0)</td><td align="center" valign="middle" >4 (0.2)</td><td align="center" valign="middle" >26 (0.8)</td></tr><tr><td align="center" valign="middle"  rowspan="3"  >Total</td><td align="center" valign="middle" >B</td><td align="center" valign="middle" >220 (7.5)</td><td align="center" valign="middle" >323 (11.0)</td><td align="center" valign="middle" >267 (9.1)</td><td align="center" valign="middle" >269 (9.1)</td><td align="center" valign="middle" >308 (10.5)</td><td align="center" valign="middle" >1387 (47.1)</td></tr><tr><td align="center" valign="middle" >G</td><td align="center" valign="middle" >244 (8.3)</td><td align="center" valign="middle" >270 (9.2)</td><td align="center" valign="middle" >325 (11.0)</td><td align="center" valign="middle" >327 (11.1)</td><td align="center" valign="middle" >391 (13.3)</td><td align="center" valign="middle" >1557 (52.9)</td></tr><tr><td align="center" valign="middle" >T</td><td align="center" valign="middle" >464 (15.8)</td><td align="center" valign="middle" >593 (20.1)</td><td align="center" valign="middle" >592 (20.1)</td><td align="center" valign="middle" >596 (20.2)</td><td align="center" valign="middle" >699 (23.7)</td><td align="center" valign="middle" >2944 (100.0)</td></tr></tbody></table></table-wrap><p>B = Boys; G = Girls; Total = B + G.</p><table-wrap id="table2" ><label><xref ref-type="table" rid="table2">Table 2</xref></label><caption><title> Prevalence of STH by district and age group</title></caption><table><tbody><thead><tr><th align="center" valign="middle"  rowspan="2"  ></th><th align="center" valign="middle" >7 - 9 years</th><th align="center" valign="middle" >10 - 12 years</th><th align="center" valign="middle" >13 - 15 years</th><th align="center" valign="middle" >≥15 years</th><th align="center" valign="middle" >Total</th></tr></thead><tr><td align="center" valign="middle" >n/N (%)</td><td align="center" valign="middle" >n/N (%)</td><td align="center" valign="middle" >n/N (%)</td><td align="center" valign="middle" >n/N (%)</td><td align="center" valign="middle" >n/N (%)</td></tr><tr><td align="center" valign="middle" >D1</td><td align="center" valign="middle" >1/136 (0.7)</td><td align="center" valign="middle" >3/215 (14.0)</td><td align="center" valign="middle" >2/107 (1.9)</td><td align="center" valign="middle" >1/6 (16.7)</td><td align="center" valign="middle" >7/464 (1.5)</td></tr><tr><td align="center" valign="middle" >D2</td><td align="center" valign="middle" >6/142 (4.2)</td><td align="center" valign="middle" >29/325 (8.9)</td><td align="center" valign="middle" >15/118 (12.7)</td><td align="center" valign="middle" >1/8 (12.5)</td><td align="center" valign="middle" >51/593 (8.6)</td></tr><tr><td align="center" valign="middle" >D3</td><td align="center" valign="middle" >5/183 (2.7)</td><td align="center" valign="middle" >18/307 (5.9)</td><td align="center" valign="middle" >10/95 (10.5)</td><td align="center" valign="middle" >0/7 (0.0)</td><td align="center" valign="middle" >33/592 (5.6)</td></tr><tr><td align="center" valign="middle" >D4</td><td align="center" valign="middle" >4/160 (2.5)</td><td align="center" valign="middle" >15/310 (4.8)</td><td align="center" valign="middle" >9/125 (7.2)</td><td align="center" valign="middle" >0/1 (0.0)</td><td align="center" valign="middle" >28/596 (4.7)</td></tr><tr><td align="center" valign="middle" >D5</td><td align="center" valign="middle" >5/204 (2.5)</td><td align="center" valign="middle" >19/350 (5.4)</td><td align="center" valign="middle" >3/141 (2.1)</td><td align="center" valign="middle" >2/4 (5.0)</td><td align="center" valign="middle" >29/699 (4.1)</td></tr><tr><td align="center" valign="middle" >Total</td><td align="center" valign="middle" >21/825 (2.5)</td><td align="center" valign="middle" >84/1507 (5.6)</td><td align="center" valign="middle" >39/586 (6.7)</td><td align="center" valign="middle" >4/26 (15.4)</td><td align="center" valign="middle" >148/2944 (5.0)</td></tr></tbody></table></table-wrap><p>N = Number of pupils surveyed; D = district; n = number of positive cases; P &lt; 0.0001 (age); P &lt; 0.0001 (district).</p><p>Among pupils positive for STH, hookworm represented 68.2% (101/148) of infections. Other helminths identified were Schistosoma mansoni (n = 6; 0.20%), Hymenolepis nana (n = 3; 0.10%), Taenia sp (n = 2; 0.07%) and Dicrocoelium dendriticum (n = 1; 0.03%). Intensity of infection was mild in more than 83% of STH positive cases and in 89.1% hookworm cases. Among children with hookworm infection, the egg count median per gram of stool was 239 [95% CI 203 - 275] with extremes of 24 and 54,720. There were insufficient numbers of A. lumbricoides and T. trichiura infections to analyze intensity of infection.</p></sec><sec id="s3_3"><title>3.3. Prevalence of Intestinal Protozoa</title><p>Stool samples from 3<sup>rd</sup> and 6<sup>th</sup> grade students (1465 of the 2944 students) were examined for intestinal protozoa; 52.2% (N = 765) were positive. Commensal amoebae were the predominant intestinal protozoa identified (22.7%). There was no significant difference in the prevalence of intestinal protozoa by age (p = 0.1968), grade (p = 0.1194) (<xref ref-type="table" rid="table3">Table 3</xref>) or sex (p = 0.2984) (<xref ref-type="table" rid="table3">Table 3</xref>) of the children although prevalence decreased with age among children less than 15 years old.</p><p>Children in District N˚2 were significantly more likely to have intestinal protozoa than were the others (55.1% in district N˚2; p = 0.0412) (<xref ref-type="fig" rid="fig1">Figure 1</xref>).</p><p>Among the intestinal protozoa found, the most common pathogenic protozoa wereEntamoeba histolytica/dispar/moshkovskii,Giardia lamblia and Trichomonas intestinalis with an overall prevalence of 17.6% (<xref ref-type="table" rid="table4">Table 4</xref>).</p><table-wrap id="table3" ><label><xref ref-type="table" rid="table3">Table 3</xref></label><caption><title> Prevalence of intestinal protozoa by level of education and gender</title></caption><table><tbody><thead><tr><th align="center" valign="middle"  rowspan="2"  ></th><th align="center" valign="middle" >Boys</th><th align="center" valign="middle" >Girls</th><th align="center" valign="middle" >Total</th></tr></thead><tr><td align="center" valign="middle" >n/N (%)</td><td align="center" valign="middle" >n/N (%)</td><td align="center" valign="middle" >n/N (%)</td></tr><tr><td align="center" valign="middle" >3<sup>rd</sup> grade</td><td align="center" valign="middle" >205/356 (57.6)</td><td align="center" valign="middle" >201/393 (51.1)</td><td align="center" valign="middle" >406/749 (54.2)</td></tr><tr><td align="center" valign="middle" >6<sup>th</sup> grade</td><td align="center" valign="middle" >160/324 (49.4)</td><td align="center" valign="middle" >199/392 (50.8)</td><td align="center" valign="middle" >359/716 (50.1)</td></tr><tr><td align="center" valign="middle" >Total</td><td align="center" valign="middle" >365/680 (53.7)</td><td align="center" valign="middle" >400/785 (50.9)</td><td align="center" valign="middle" >765/1465 (52.2)</td></tr></tbody></table></table-wrap><p>N = number of children surveyed; n = number of positive cases; p = 0.1194 (grade); p = 0.2984 (sex).</p><table-wrap id="table4" ><label><xref ref-type="table" rid="table4">Table 4</xref></label><caption><title> Species of intestinal protozoa identified</title></caption><table><tbody><thead><tr><th align="center" valign="middle" ></th><th align="center" valign="middle" >Parasites</th><th align="center" valign="middle" >n</th><th align="center" valign="middle" >Prevalence (%)</th></tr></thead><tr><td align="center" valign="middle"  rowspan="5"  >Amoebae</td><td align="center" valign="middle" >Entamoeba histolytica/dispar/moshkovskii</td><td align="center" valign="middle" >34</td><td align="center" valign="middle" >2.3</td></tr><tr><td align="center" valign="middle" >Entamoeba coli</td><td align="center" valign="middle" >241</td><td align="center" valign="middle" >16.5</td></tr><tr><td align="center" valign="middle" >Entamoeba hartmanni</td><td align="center" valign="middle" >10</td><td align="center" valign="middle" >0.7</td></tr><tr><td align="center" valign="middle" >Endolimax nana</td><td align="center" valign="middle" >7</td><td align="center" valign="middle" >0.5</td></tr><tr><td align="center" valign="middle" >Pseudolimax butschlii</td><td align="center" valign="middle" >60</td><td align="center" valign="middle" >4.1</td></tr><tr><td align="center" valign="middle"  rowspan="3"  >Flagellates</td><td align="center" valign="middle" >Giardia lamblia</td><td align="center" valign="middle" >168</td><td align="center" valign="middle" >11.5</td></tr><tr><td align="center" valign="middle" >Trichomonas intestinalis</td><td align="center" valign="middle" >55</td><td align="center" valign="middle" >3.8</td></tr><tr><td align="center" valign="middle" >Chilomastix mesnili</td><td align="center" valign="middle" >13</td><td align="center" valign="middle" >0.9</td></tr><tr><td align="center" valign="middle" >Others</td><td align="center" valign="middle" >Blastocystis hominis</td><td align="center" valign="middle" >160</td><td align="center" valign="middle" >10.9</td></tr><tr><td align="center" valign="middle" >Total</td><td align="center" valign="middle" ></td><td align="center" valign="middle" >765</td><td align="center" valign="middle" >52.2</td></tr></tbody></table></table-wrap><p>n = number of positive cases.</p><p>A few cases of polyparasitism were noted, including helminth-helminth, protozoan-protozoan and helminth-protozoa association respectively in 1.35% (2/148), 12.2% (93/765) and 2.38% (35/1465) of cases.</p></sec></sec><sec id="s4"><title>4. Discussion</title><sec id="s4_1"><title>4.1. Prevalence of STH</title><p>Togo’s national program for the integrated control neglected tropical disease, launched in 2009, did not conduct MDA with albendazole for STH in Lom&#233;-commune because the area was considered to be at low risk based on available data. However, to ensure that all children at risk benefit from preventive chemotherapy with albendazole, it was important to measure STH prevalence in this region, where 1/7 of Togo’s population lives. The low overall prevalence of STH of 5.0% found in this study confirms the results previously obtained by Vovor and al. in 2008 in this same region (7.3%) [<xref ref-type="bibr" rid="scirp.110185-ref13">13</xref>] but contrasts with the 32.1% found by Dorkenoo and al. [<xref ref-type="bibr" rid="scirp.110185-ref5">5</xref>] in 2009 during the nationwide evaluation which covered the five regions of Togo outside of Lom&#233;-commune. Results from the present study and from Vovor et al. [<xref ref-type="bibr" rid="scirp.110185-ref13">13</xref>] corroborate the trend towards low STH prevalence in urban areas. Indeed, urban areas often have a relatively high level of sanitation maintained by local authorities and a high literacy rate, and residents may have a better understanding of, and compliance with, appropriate infection prevention measures. Poor environmental sanitation, limited access to latrines, unsafe water supply, low level of knowledge and practices of good individual hygiene, and low standard of living are often mentioned as major factors for the high prevalence of intestinal parasites among rural as compared to urban dwellers [<xref ref-type="bibr" rid="scirp.110185-ref14">14</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref15">15</xref>]. Tchuem Tchuent&#233; et al. in Cameroon in 2012 highlighted this, finding a significantly higher prevalence of STH in rural and peri-urban areas than in urban areas [<xref ref-type="bibr" rid="scirp.110185-ref16">16</xref>]. Our results also showed that the highest district-level prevalence of STH in Lom&#233; commune (8.6%) was indeed found in the district covering the peri-urban area of the capital. In contrast, Phiri et al. in Malawi in 2016 reported a significantly higher overall prevalence in urban than in rural areas (16.5% vs. 3.6%; p &lt; 0.001) [<xref ref-type="bibr" rid="scirp.110185-ref17">17</xref>]. In this Malawian urban community, risk factors included having pools of water/sewage around houses (OR = 3.0; CI = 1.4 - 6.5), not wearing shoes (OR = 7.1; CI = 2.7 - 19.2), not attending school (OR = 2.8; CI = 1.2 - 6.5), mothers having only 4 - 8 years of education (OR = 5.2; CI = 2.0 - 14.0), and mothers being below 35 years of age (OR = 4.09; CI = 1.39 - 16.28) [<xref ref-type="bibr" rid="scirp.110185-ref17">17</xref>]. In a Togolese study analyzing water, sanitation and hygiene (WASH) conditions in 2015, only unimproved drinking water was found to be significantly associated with the presence or absence of hookworms in an individual; however, intensity of infection (number eggs per gram of feces) was associated with availability of unimproved drinking water, availability of improved drinking water either on or off school grounds, having a handwashing station with water available, and access to a sex separate non-private or private latrine [<xref ref-type="bibr" rid="scirp.110185-ref18">18</xref>]. The variable distribution of these infections is therefore not always related to the urban or rural character of the survey area but may rather be related to the state of its environmental sanitation [<xref ref-type="bibr" rid="scirp.110185-ref15">15</xref>]. In addition, other factors could explain the disparity in results, especially the age of the subjects surveyed, their underlying state of health, socio-economic status and the parasitological tool and method used to identify the helminths.</p><p>The low STH prevalence in our study could also be due to the systematic deworming done in routine practice in the paediatric services of the health centers of Lom&#233;.</p><p>The STH prevalence varied according to sex: 5.7% in boys versus 4.4% in girls (p = 0.049). This male predominance has been reported in several studies [<xref ref-type="bibr" rid="scirp.110185-ref19">19</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref20">20</xref>], while others have noted a female predominance [<xref ref-type="bibr" rid="scirp.110185-ref8">8</xref>].</p><p>STH prevalence in our study also increased significantly with age (p = 0.0001) and consequently with grade level. This result is likely due, in part, to the residual impact on the younger age groups of the albendazole deworming campaigns organized annually by the national nutrition program, with the support of UNICEF, for children under 5 years of age [<xref ref-type="bibr" rid="scirp.110185-ref21">21</xref>].</p><p>Hookworm was the most frequently identified helminth (68.2% of the 148 positive cases) with a prevalence of 3.4% in our study; the same observation was made elsewhere in Togo, Benin and C&#244;te d’Ivoire, although the rates were much higher [<xref ref-type="bibr" rid="scirp.110185-ref5">5</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref22">22</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref23">23</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref24">24</xref>]. In this study, very low prevalence of A. lumbricoides andT. trichiura was found (0.8% for each species), confirming the results of Dorkenoo et al. in Togo in 2009 and 2015 [<xref ref-type="bibr" rid="scirp.110185-ref5">5</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref8">8</xref>]. However, these results contrast with those of N’diaye et al. [<xref ref-type="bibr" rid="scirp.110185-ref20">20</xref>] in Senegal where A. lumbricoides and T. trichiura were the predominant species with a prevalence of 60% and 25.6% respectively. Local ecology and the history of distribution of ivermectin in countries co-endemic for onchocerciasis may play a role in this disparity.</p><p>The low prevalence and intensity of infestation observed in our study support the decision not to extend mass treatment with albendazole to this region of Lom&#233;-commune.</p></sec><sec id="s4_2"><title>4.2. Prevalence of Protozoa</title><p>The nested survey of intestinal protozoa in 3<sup>rd</sup> and 6<sup>th</sup> grade children was included to provide information on the prevalence of these infections, which have not previously been examined in this region; 52.2% of pupils surveyed were positive for at least one protozoan in our study. Our prevalence is higher than the 34.7% prevalence found among children under 5 years of age in South Africa [<xref ref-type="bibr" rid="scirp.110185-ref25">25</xref>] and 25.2% in Rwanda [<xref ref-type="bibr" rid="scirp.110185-ref26">26</xref>]. This difference is likely due to the fact that in our study all identified parasites (pathogenic and commensal protozoa) were accounted for, while the other authors focused their evaluations only on pathogen species. However, the prevalence of protozoa in Togo is lower than that reported in some Maghreb countries: 96.5% in Sfax in Tunisia [<xref ref-type="bibr" rid="scirp.110185-ref27">27</xref>] and 88.3% in Kenitra in Morocco [<xref ref-type="bibr" rid="scirp.110185-ref28">28</xref>]. This difference could be related to the diagnostic techniques (parasite concentration and/or molecular or immunological tools) used in these other studies versus the direct examination technique used in our study.</p><p>There was no gender difference in prevalence of protozoal infection in our study, as was also found by Sacolo-Gwebu in South Africa and Elqai in Morocco [<xref ref-type="bibr" rid="scirp.110185-ref25">25</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref28">28</xref>]; there was a non-significant trend toward decreased prevalence in older grades, from 54.2% for the 3<sup>rd</sup> grade group to 50.1% for the 6<sup>th</sup> grade group (p = 0.1194). This decrease in infection may be due to older children practicing better individual hygiene: washing their hands, wearing shoes, losing interest in dirty games.</p><p>Prevalence of intestinal protozoa varied by district; the highest rates were observed in peri-urban areas (districts 2 and 3) where access to latrines is poorer and where individual and collective hygiene practices are less frequently observed.</p><p>The pathogenic species Entamoeba histolytica/dispar/mishkovskii, Giardia intestinalis and Trichomonas intestinalis were found at relatively low rates, 2.3%, 11.5% and 3.8% respectively. Our results are similar to those of Chekhrouhou [<xref ref-type="bibr" rid="scirp.110185-ref27">27</xref>] who reported these species in 2.2%, 17% and 1.5% respectively, and those of Ghenghesh in Libya, for the period 2000-2015, who noted 6% of E. histolytica/dispar/moshkovskii, 2% of G. lamblia and 0.9% of Cryptosporidium spp. [<xref ref-type="bibr" rid="scirp.110185-ref29">29</xref>]. Much higher prevalence of E. histolytica/dispar/moshkovskii has been described worldwide [<xref ref-type="bibr" rid="scirp.110185-ref29">29</xref>] [<xref ref-type="bibr" rid="scirp.110185-ref30">30</xref>]; the most commonly identified commensal species were E. nana and Entamoeba coli, with prevalence of 65.5% and 62.3%, respectively [<xref ref-type="bibr" rid="scirp.110185-ref30">30</xref>], similar to our study where E. coli was the most prevalent commensal amoebae (16.5%). In South Africa, Samie et al. were able to differentiate between the three species of the E. histolytica complex in 170 samples using the Polymerase Chain Reaction (PCR) technique and noted 15.9% E. moshkovskii, 14.7% E. dispar and 4.1% E. histolytica [<xref ref-type="bibr" rid="scirp.110185-ref31">31</xref>]. This finding suggests that the proportion of pathogenic species in our study might have been much lower had we used PCR to differentiate the non-pathogenic and pathogenic species of E. histolytica complex.</p><p>The prevalence of pathogenic intestinal protozoa in our study does not constitute a public health problem in the Lom&#233; commune health region, similar to our findings for STH.</p></sec></sec><sec id="s5"><title>5. Conclusion</title><p>The low prevalence of STH among pupils in the Lom&#233;-commune health region shows that, despite variability between districts and schools, with urban areas having relatively lower prevalence than more rural areas, the WHO threshold for implementing albendazole mass drug administration is not reached. Low prevalence of pathogenic intestinal protozoa was also found. Intestinal parasites and especially STH, therefore, do not appear to constitute a significant public health problem in the Lom&#233;-commune region. Nonetheless, SAC in this region should be treated three times during their primary school period in accordance with the WHO guidelines and emphasis placed on hygiene education and awareness-raising for the elimination of these intestinal parasites in Togo.</p></sec><sec id="s6"><title>Limitations</title><p>This work is submitted for publication after several years as a 5-year evaluative study was planned in 2018. Due to lack of funding it has not yet taken place. It was therefore imperative for us to report on the first stage of the project conducted in 2013. The data presented in this manuscript may no longer represent the current situation of the prevalence of these potentially evolving STH, but the study had the merit of showing that this health region where the Togolese capital is located does not need MDA of albendazole to SAC.</p></sec><sec id="s7"><title>Conflicts of Interest</title><p>The authors declare no conflicts of interest regarding the publication of this paper.</p></sec><sec id="s8"><title>Cite this paper</title><p>Dorkenoo, M.A., Agbeko, F., Dokoto, H., Plate, D., Fiawoo, M., Yakpa, K., Sossou, E., Sognikin, S.K., Gbadoe, A.D. and Bronzan, R. (2021) Prevalence of Soil-Transmitted Helminths and Intestinal Protozoa among School Children in Lome, Togo. Open Journal of Pediatrics, 11, 313-328. https://doi.org/10.4236/ojped.2021.112029</p></sec><sec id="s9"><title>Questionnaire 1</title><p>District:........... Ecole:............................... 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