An Epidemiologic Review of Enteropathogens in Gaborone, Botswana: Shifting Patterns of Resistance in an HIV Endemic Region
Identifieur interne : 002B36 ( Pmc/Corpus ); précédent : 002B35; suivant : 002B37An Epidemiologic Review of Enteropathogens in Gaborone, Botswana: Shifting Patterns of Resistance in an HIV Endemic Region
Auteurs : Jack S. Rowe ; Samir S. Shah ; Stephen Motlhagodi ; Margaret Bafana ; Ephraim Tawanana ; Hong T. Truong ; Sarah M. Wood ; Nicola M. Zetola ; Andrew P. SteenhoffSource :
- PLoS ONE [ 1932-6203 ] ; 2010.
Abstract
The epidemiology of diarrheal disease in Botswana, an HIV endemic region, is largely unknown. Our primary objective was to characterize the prevalent bacterial and parasitic enteropathogens in Gaborone, Botswana. Secondary objectives included determining corresponding antimicrobial resistance patterns and the value of stool white and red blood cells for predicting bacterial and parasitic enteropathogens.
A retrospective cross-sectional study examined laboratory records of stool
specimens analyzed by the Botswana National Health Laboratory in Gaborone,
Botswana from February 2003 through July 2008. In 4485 specimens the median
subject age was 23 [interquartile range 1.6–34]
years. Overall, 14.4% (644 of 4485) of samples yielded a
pathogen. Bacteria alone were isolated in 8.2% (367 of 4485),
parasites alone in 5.6% (253 of 4485) and both in 0.5%
(24 of 4485) of samples. The most common bacterial pathogens were
Most gastroenteritis stools were culture and microscopy negative suggesting
that viral pathogens were the majority etiologic agents in this Botswana
cohort.
Url:
DOI: 10.1371/journal.pone.0010924
PubMed: 20543877
PubMed Central: 2881529
Links to Exploration step
PMC:2881529Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">An Epidemiologic Review of Enteropathogens in Gaborone, Botswana:
Shifting Patterns of Resistance in an HIV Endemic Region</title><author><name sortKey="Rowe, Jack S" sort="Rowe, Jack S" uniqKey="Rowe J" first="Jack S." last="Rowe">Jack S. Rowe</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Shah, Samir S" sort="Shah, Samir S" uniqKey="Shah S" first="Samir S." last="Shah">Samir S. Shah</name><affiliation><nlm:aff id="aff2"><addr-line>University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><addr-line>The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Motlhagodi, Stephen" sort="Motlhagodi, Stephen" uniqKey="Motlhagodi S" first="Stephen" last="Motlhagodi">Stephen Motlhagodi</name><affiliation><nlm:aff id="aff3"><addr-line>Botswana National Health Laboratory, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Bafana, Margaret" sort="Bafana, Margaret" uniqKey="Bafana M" first="Margaret" last="Bafana">Margaret Bafana</name><affiliation><nlm:aff id="aff3"><addr-line>Botswana National Health Laboratory, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Tawanana, Ephraim" sort="Tawanana, Ephraim" uniqKey="Tawanana E" first="Ephraim" last="Tawanana">Ephraim Tawanana</name><affiliation><nlm:aff id="aff3"><addr-line>Botswana National Health Laboratory, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Truong, Hong T" sort="Truong, Hong T" uniqKey="Truong H" first="Hong T." last="Truong">Hong T. Truong</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wood, Sarah M" sort="Wood, Sarah M" uniqKey="Wood S" first="Sarah M." last="Wood">Sarah M. Wood</name><affiliation><nlm:aff id="aff5"><addr-line>The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zetola, Nicola M" sort="Zetola, Nicola M" uniqKey="Zetola N" first="Nicola M." last="Zetola">Nicola M. Zetola</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Steenhoff, Andrew P" sort="Steenhoff, Andrew P" uniqKey="Steenhoff A" first="Andrew P." last="Steenhoff">Andrew P. Steenhoff</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><addr-line>The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">20543877</idno><idno type="pmc">2881529</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2881529</idno><idno type="RBID">PMC:2881529</idno><idno type="doi">10.1371/journal.pone.0010924</idno><date when="2010">2010</date><idno type="wicri:Area/Pmc/Corpus">002B36</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002B36</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">An Epidemiologic Review of Enteropathogens in Gaborone, Botswana:
Shifting Patterns of Resistance in an HIV Endemic Region</title><author><name sortKey="Rowe, Jack S" sort="Rowe, Jack S" uniqKey="Rowe J" first="Jack S." last="Rowe">Jack S. Rowe</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Shah, Samir S" sort="Shah, Samir S" uniqKey="Shah S" first="Samir S." last="Shah">Samir S. Shah</name><affiliation><nlm:aff id="aff2"><addr-line>University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><addr-line>The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Motlhagodi, Stephen" sort="Motlhagodi, Stephen" uniqKey="Motlhagodi S" first="Stephen" last="Motlhagodi">Stephen Motlhagodi</name><affiliation><nlm:aff id="aff3"><addr-line>Botswana National Health Laboratory, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Bafana, Margaret" sort="Bafana, Margaret" uniqKey="Bafana M" first="Margaret" last="Bafana">Margaret Bafana</name><affiliation><nlm:aff id="aff3"><addr-line>Botswana National Health Laboratory, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Tawanana, Ephraim" sort="Tawanana, Ephraim" uniqKey="Tawanana E" first="Ephraim" last="Tawanana">Ephraim Tawanana</name><affiliation><nlm:aff id="aff3"><addr-line>Botswana National Health Laboratory, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Truong, Hong T" sort="Truong, Hong T" uniqKey="Truong H" first="Hong T." last="Truong">Hong T. Truong</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Wood, Sarah M" sort="Wood, Sarah M" uniqKey="Wood S" first="Sarah M." last="Wood">Sarah M. Wood</name><affiliation><nlm:aff id="aff5"><addr-line>The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Zetola, Nicola M" sort="Zetola, Nicola M" uniqKey="Zetola N" first="Nicola M." last="Zetola">Nicola M. Zetola</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation></author><author><name sortKey="Steenhoff, Andrew P" sort="Steenhoff, Andrew P" uniqKey="Steenhoff A" first="Andrew P." last="Steenhoff">Andrew P. Steenhoff</name><affiliation><nlm:aff id="aff1"><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><addr-line>The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2010">2010</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>The epidemiology of diarrheal disease in Botswana, an HIV endemic region, is
largely unknown. Our primary objective was to characterize the prevalent
bacterial and parasitic enteropathogens in Gaborone, Botswana. Secondary
objectives included determining corresponding antimicrobial resistance
patterns and the value of stool white and red blood cells for predicting
bacterial and parasitic enteropathogens.</p></sec><sec><title>Methodology/Principal Findings</title><p>A retrospective cross-sectional study examined laboratory records of stool
specimens analyzed by the Botswana National Health Laboratory in Gaborone,
Botswana from February 2003 through July 2008. In 4485 specimens the median
subject age was 23 [interquartile range 1.6–34]
years. Overall, 14.4% (644 of 4485) of samples yielded a
pathogen. Bacteria alone were isolated in 8.2% (367 of 4485),
parasites alone in 5.6% (253 of 4485) and both in 0.5%
(24 of 4485) of samples. The most common bacterial pathogens were
<italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp.,
isolated from 4.0% (180 of 4485) and 3.9% (175 of
4485) of specimens, respectively. <italic>Escherichia coli</italic> (22 of
4485) and <italic>Campylobacter</italic> spp. (22 of 4485) each accounted
for 0.5% of pathogens. Comparing antimicrobial resistance among
<italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp.
between two periods, February 2003 to February 2004 and July 2006 to July
2008, revealed an increase in ampicillin resistance among
<italic>Shigella</italic> spp. from 43% to 83%
(p<0.001). Among <italic>Salmonella</italic> spp., resistance to
chloramphenicol decreased from 56% to 6%
(p<0.001). The absence of stool white and red blood cells correlated
with a high specificity and negative predictive value.</p></sec><sec><title>Conclusions/Significance</title><p>Most gastroenteritis stools were culture and microscopy negative suggesting
that viral pathogens were the majority etiologic agents in this Botswana
cohort. <italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp.
were the most common bacteria; <italic>Isospora</italic> spp. and
<italic>Cryptosporidium</italic> spp. were the most common parasites.
Resistance to commonly used antimicrobials is high and should be closely
monitored.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Bryce, J" uniqKey="Bryce J">J Bryce</name></author><author><name sortKey="Boschi Pinto, C" uniqKey="Boschi Pinto C">C Boschi-Pinto</name></author><author><name sortKey="Shibuya, K" uniqKey="Shibuya K">K Shibuya</name></author><author><name sortKey="Black, Re" uniqKey="Black R">RE Black</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Obimbo, Em" uniqKey="Obimbo E">EM Obimbo</name></author><author><name sortKey="Mbori Ngacha, Da" uniqKey="Mbori Ngacha D">DA Mbori-Ngacha</name></author><author><name sortKey="Ochieng, Jo" uniqKey="Ochieng J">JO Ochieng</name></author><author><name sortKey="Richardson, Ba" uniqKey="Richardson B">BA Richardson</name></author><author><name sortKey="Otieno, Pa" uniqKey="Otieno P">PA Otieno</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bachou, H" uniqKey="Bachou H">H 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">20543877</article-id><article-id pub-id-type="pmc">2881529</article-id><article-id pub-id-type="publisher-id">10-PONE-RA-15339R1</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0010924</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline"><subject>Infectious Diseases</subject><subject>Infectious Diseases/Antimicrobials and Drug Resistance</subject><subject>Infectious Diseases/Epidemiology and Control of Infectious Diseases</subject><subject>Infectious Diseases/Gastrointestinal Infections</subject><subject>Infectious Diseases/HIV Infection and AIDS</subject></subj-group></article-categories><title-group><article-title>An Epidemiologic Review of Enteropathogens in Gaborone, Botswana:
Shifting Patterns of Resistance in an HIV Endemic Region</article-title><alt-title alt-title-type="running-head">Enteropathogens in Botswana</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Rowe</surname><given-names>Jack S.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Shah</surname><given-names>Samir S.</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Motlhagodi</surname><given-names>Stephen</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bafana</surname><given-names>Margaret</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Tawanana</surname><given-names>Ephraim</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Truong</surname><given-names>Hong T.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wood</surname><given-names>Sarah M.</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zetola</surname><given-names>Nicola M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Steenhoff</surname><given-names>Andrew P.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Botswana-UPenn Partnership, Gaborone, Botswana</addr-line></aff><aff id="aff2"><label>2</label><addr-line>University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, United States of America</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Botswana National Health Laboratory, Gaborone, Botswana</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Princess Marina Hospital, Gaborone, Botswana</addr-line></aff><aff id="aff5"><label>5</label><addr-line>The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Myer</surname><given-names>Landon</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1">University of Cape Town, South Africa</aff><author-notes><corresp id="cor1">* E-mail: <email>steenhoff@email.chop.edu</email></corresp><fn fn-type="con"><p>Conceived and designed the experiments: JSR SSS MB HTT SMW APS. Performed the
experiments: JSR SM MB ET APS. Analyzed the data: JSR SSS NMZ APS. Wrote the
paper: JSR SSS SM MB ET HTT SMW NMZ APS.</p></fn></author-notes><pub-date pub-type="collection"><year>2010</year></pub-date><pub-date pub-type="epub"><day>2</day><month>6</month><year>2010</year></pub-date><volume>5</volume><issue>6</issue><elocation-id>e10924</elocation-id><history><date date-type="received"><day>7</day><month>1</month><year>2010</year></date><date date-type="accepted"><day>23</day><month>4</month><year>2010</year></date></history><permissions><copyright-statement>Rowe 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.</copyright-statement></permissions><abstract><sec><title>Background</title><p>The epidemiology of diarrheal disease in Botswana, an HIV endemic region, is
largely unknown. Our primary objective was to characterize the prevalent
bacterial and parasitic enteropathogens in Gaborone, Botswana. Secondary
objectives included determining corresponding antimicrobial resistance
patterns and the value of stool white and red blood cells for predicting
bacterial and parasitic enteropathogens.</p></sec><sec><title>Methodology/Principal Findings</title><p>A retrospective cross-sectional study examined laboratory records of stool
specimens analyzed by the Botswana National Health Laboratory in Gaborone,
Botswana from February 2003 through July 2008. In 4485 specimens the median
subject age was 23 [interquartile range 1.6–34]
years. Overall, 14.4% (644 of 4485) of samples yielded a
pathogen. Bacteria alone were isolated in 8.2% (367 of 4485),
parasites alone in 5.6% (253 of 4485) and both in 0.5%
(24 of 4485) of samples. The most common bacterial pathogens were
<italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp.,
isolated from 4.0% (180 of 4485) and 3.9% (175 of
4485) of specimens, respectively. <italic>Escherichia coli</italic> (22 of
4485) and <italic>Campylobacter</italic> spp. (22 of 4485) each accounted
for 0.5% of pathogens. Comparing antimicrobial resistance among
<italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp.
between two periods, February 2003 to February 2004 and July 2006 to July
2008, revealed an increase in ampicillin resistance among
<italic>Shigella</italic> spp. from 43% to 83%
(p<0.001). Among <italic>Salmonella</italic> spp., resistance to
chloramphenicol decreased from 56% to 6%
(p<0.001). The absence of stool white and red blood cells correlated
with a high specificity and negative predictive value.</p></sec><sec><title>Conclusions/Significance</title><p>Most gastroenteritis stools were culture and microscopy negative suggesting
that viral pathogens were the majority etiologic agents in this Botswana
cohort. <italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp.
were the most common bacteria; <italic>Isospora</italic> spp. and
<italic>Cryptosporidium</italic> spp. were the most common parasites.
Resistance to commonly used antimicrobials is high and should be closely
monitored.</p></sec></abstract><counts><page-count count="6"></page-count></counts></article-meta></front><body><sec id="s1"><title>Introduction</title><p>Diarrheal disease is a serious cause of mortality and morbidity in Sub-Saharan
Africa, accounting for an estimated 16% of deaths in Africa among
children <5 years of age<xref ref-type="bibr" rid="pone.0010924-Bryce1">[1]</xref>. The burden of diarrheal disease is amplified by
Africa's human immunodeficiency virus (HIV) epidemic, as diarrheal disease
is a major cause of mortality and morbidity among HIV-infected patients and can
intensify HIV-related wasting and malnutrition <xref ref-type="bibr" rid="pone.0010924-Obimbo1">[2]</xref>. HIV-infected subjects
have a predilection for chronic diarrhea, which is most pronounced in those with
lowest CD4+ cell counts <xref ref-type="bibr" rid="pone.0010924-Bachou1">[3]</xref>, <xref ref-type="bibr" rid="pone.0010924-Brink1">[4]</xref>.</p><p>A broad range of etiologic agents are responsible for acute and chronic diarrheal
disease, and the prevalence of such agents varies greatly by geographic region,
season, patient age, immune status, and socioeconomic conditions. The dynamic
variability of etiologic agents has been shown in studies throughout southern Africa
<xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Cranendonk1">[6]</xref>, <xref ref-type="bibr" rid="pone.0010924-KhumaloNgwenya1">[7]</xref>, <xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Mwansa1">[9]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Reither1">[10]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Samie1">[11]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Temu1">[12]</xref>.
Several Sub-Saharan African studies have also indicated a high prevalence of
resistance to commonly used antimicrobials, such as ampicillin and
trimethoprim-sulfamethoxazole <xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>, <xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>, <xref ref-type="bibr" rid="pone.0010924-Mwansa1">[9]</xref>, <xref ref-type="bibr" rid="pone.0010924-Temu1">[12]</xref>. However,
resistance patterns are often regionally-specific, and there is little data
describing how these patterns have changed over time. To date, there is limited data
regarding the epidemiology of diarrheal disease in Gaborone, Botswana, an HIV
endemic region.</p><p>The primary objective of this study was to determine the prevalence of bacterial and
parasitic enteropathogens in Gaborone, Botswana in stool samples from both inpatient
and outpatient adult and pediatric populations. Secondary objectives were to
describe antimicrobial susceptibilities of the most frequently occurring bacterial
pathogens, <italic>Salmonella</italic> spp. and <italic>Shigella</italic> spp., and
to determine the sensitivity, specificity, positive predictive value and negative
predictive value of stool white blood cells (WBC) and red blood cells (RBC) for
bacterial and parasitic enteropathogens.</p></sec><sec id="s2" sec-type="methods"><title>Methods</title><sec id="s2a"><title>Ethics Statement</title><p>This study was reviewed and approved by the institutional review boards of the
Botswana Ministry of Health (Gaborone, Botswana), Princess Marina Hospital
(Gaborone, Botswana), and The Children's Hospital of Philadelphia
(Philadelphia PA, USA). A waiver of informed consent was granted by all review
boards given that the study represented a de-identified, retrospective study of
routine clinical practice with no more than minimal risk to subjects.</p></sec><sec id="s2b"><title>Study Design, Setting, and Participants</title><p>A retrospective, cross-sectional study of stool specimen records collected
between February 1, 2003 and July 31, 2008 was performed at the Botswana
National Health Laboratory (BNHL) in Gaborone, Botswana. The BNHL, which serves
a population of 500,000, is the reference microbiology laboratory for the public
health facilities in and those surrounding Gaborone, Botswana. Stool samples
received from Princess Marina Hospital (PMH), the largest tertiary care referral
center in Botswana, as well as from clinics and smaller hospitals within a 30 km
radius of Gaborone were eligible for inclusion. Specimens were excluded if they
came from a patient without gastroenteritis. Botswana has the second highest
prevalence of HIV in the world. In 2007, an estimated 23.9% of
Batswana aged 15–49 years were HIV positive <xref ref-type="bibr" rid="pone.0010924-Organization1">[13]</xref>.</p></sec><sec id="s2c"><title>Microbiology Methods</title><p>Stool samples were subjected to microscopy, culture, and antimicrobial
susceptibility testing. Routine laboratory practice for stool samples at the
BNHL during the study period followed a standard operating procedure including a
24 hour turn-around-time for stool microscopy and processing of all stool
samples within 24 hours of collection. All samples were assessed by a qualified
laboratory technologist who was supervised by a laboratory scientist. Weekend
coverage included a technologist on duty until 4 pm each day. Antimicrobial
susceptibility patterns of isolates were determined by disk-diffusion method
according to Clinical Laboratory Standards Institute (CLSI) guidelines<xref ref-type="bibr" rid="pone.0010924-CLSI1">[14]</xref>.
Prior to October 2003, BNHL routinely tested stool <italic>Salmonella</italic>spp. and <italic>Shigella</italic> spp. for susceptibility to ampicillin,
trimethoprim-sulfamethoxazole, gentamicin, trimethoprim, tetracycline,
cefotaxime, and ampicillin-sulbactam. From October 2003, BNHL adopted the World
Health Organization (WHO) recommended panel of susceptibility testing to
ampicillin, trimethoprim-sulfamethoxazole, ciprofloxacin, chloramphenicol, and
nalidixic acid <xref ref-type="bibr" rid="pone.0010924-Organization2">[15]</xref>. Apart from this change in susceptibility
testing, other laboratory practices remained unchanged during the course of the
study.</p></sec><sec id="s2d"><title>Data Collection and Statistical Analysis</title><p>Electronic and paper-based records of the BNHL were reviewed to identify stool
samples meeting study inclusion criteria. Demographic data abstracted included
age, sex and, for inpatient samples only, ward location. Results of
antimicrobial susceptibility testing were recorded when available. In addition,
exposure to antibiotics in the 2 weeks before the stool sample was submitted was
recorded as antibiotic exposure in this period may have influenced the
antimicrobial susceptibilities of bacterial pathogens. Consistent and complete
stool records were available for two selected study periods: 1<sup>st</sup>February 2003 through 27<sup>th</sup> February 2004 and 1<sup>st</sup> July 2006
through 31<sup>st</sup> July 2008. For the period 28<sup>th</sup> Feb 2004 to
30<sup>th</sup> June 2006, records were available for 11 (39.3%)
of 28 months. This period contributed 308 (6.9%) of 4485 study
specimens. While the overall analysis included all specimens analyzed from
February 2003 through July 2008, the two selected study periods were compared to
determine whether changes in antimicrobial susceptibility patterns occurred over
time. Overall proportions of different pathogens found in stool were calculated
and stratified as a measure of disease burden.</p><p>Data were analyzed using STATA version 9.2 (Stata Corp., College Station, TX).
Categorical variables were compared using Fisher exact tests. Sensitivity,
specificity, positive predictive value and negative predictive value were
calculated to determine the accuracy of stool white blood cells and red blood
cells in predicting bacterial and parasitic infections.</p></sec></sec><sec id="s3"><title>Results</title><sec id="s3a"><title>Characteristics of the Study Population</title><p>During the study period, 90.4% (4485 of 4960) of stool samples met
inclusion criteria. Samples were excluded because no result was recorded (205 of
4960) or the sample came from a patient without gastroenteritis (270 of 4960).
Outpatient services (Gaborone city clinics, PMH outpatients and other clinics
within 30 km of Gaborone) accounted for 70.5% (3162 of 4485) of
specimens included in this study. Samples from inpatients at PMH accounted for
26.7% (1197 of 4485) of specimens. The location was unknown for
2.8% (126 of 4485) of specimens. The demographic characteristics of
patients from which samples were received are described in <xref ref-type="table" rid="pone-0010924-t001"><bold>Table 1</bold></xref>. The median subject age was 23 years [interquartile range:
1.6–34 years].</p><table-wrap id="pone-0010924-t001" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0010924.t001</object-id><label>Table 1</label><caption><title>Demographic Characteristics of Included Stool Specimens<xref ref-type="table-fn" rid="nt101">*</xref>.</title></caption><alternatives><graphic id="pone-0010924-t001-1" xlink:href="pone.0010924.t001"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col></colgroup><thead><tr><td align="left" rowspan="1" colspan="1"></td><td colspan="2" align="left" rowspan="1">Gender<xref ref-type="table-fn" rid="nt102">**</xref></td><td colspan="8" align="left" rowspan="1">Age Group</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Female (n = 2255)</td><td align="left" rowspan="1" colspan="1">Male (n = 1870)</td><td align="left" rowspan="1" colspan="1"><1 mo
(n = 95)</td><td align="left" rowspan="1" colspan="1">≥1 mo – <12 mo
(n = 629)</td><td align="left" rowspan="1" colspan="1">≥1 yr – <5 yr
(n = 564)</td><td align="left" rowspan="1" colspan="1">≥5 yr – <15
(n = 313)</td><td align="left" rowspan="1" colspan="1">≥15 yr – <50 yr
(n = 2166)</td><td align="left" rowspan="1" colspan="1">≥50 yr – <65 yr
(n = 185)</td><td align="left" rowspan="1" colspan="1">≥65 yr
(n = 77)</td><td align="left" rowspan="1" colspan="1">Unknown age
(n = 456)</td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><bold>Samples Positive for Bacteria
(n = 367)</bold></td><td align="left" rowspan="1" colspan="1">171 (8)</td><td align="left" rowspan="1" colspan="1">171 (9)</td><td align="left" rowspan="1" colspan="1">4 (4)</td><td align="left" rowspan="1" colspan="1">61 (10)</td><td align="left" rowspan="1" colspan="1">64 (11)</td><td align="left" rowspan="1" colspan="1">30 (10)</td><td align="left" rowspan="1" colspan="1">162 (7)</td><td align="left" rowspan="1" colspan="1">12 (6)</td><td align="left" rowspan="1" colspan="1">5 (6)</td><td align="left" rowspan="1" colspan="1">29 (6)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Samples Positive for Parasites
(n = 253)</bold></td><td align="left" rowspan="1" colspan="1">123 (5)</td><td align="left" rowspan="1" colspan="1">111 (6)</td><td align="left" rowspan="1" colspan="1">1 (1)</td><td align="left" rowspan="1" colspan="1">23 (3)</td><td align="left" rowspan="1" colspan="1">43 (8)</td><td align="left" rowspan="1" colspan="1">20 (6)</td><td align="left" rowspan="1" colspan="1">122(6)</td><td align="left" rowspan="1" colspan="1">12 (6)</td><td align="left" rowspan="1" colspan="1">2 (3)</td><td align="left" rowspan="1" colspan="1">30 (7)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Samples Positive for both Bacteria and Parasites
(n = 24)</bold></td><td align="left" rowspan="1" colspan="1">11 (<1)</td><td align="left" rowspan="1" colspan="1">12 (<1)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">5 (1)</td><td align="left" rowspan="1" colspan="1">9 (2)</td><td align="left" rowspan="1" colspan="1">1(<1)</td><td align="left" rowspan="1" colspan="1">8 (<1)</td><td align="left" rowspan="1" colspan="1">1 (<1)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Samples with no pathogen isolated
(n = 3841)</bold></td><td align="left" rowspan="1" colspan="1">1950 (86)</td><td align="left" rowspan="1" colspan="1">1576 (84)</td><td align="left" rowspan="1" colspan="1">90 (95)</td><td align="left" rowspan="1" colspan="1">540 (86)</td><td align="left" rowspan="1" colspan="1">448 (79)</td><td align="left" rowspan="1" colspan="1">262 (84)</td><td align="left" rowspan="1" colspan="1">1874 (87)</td><td align="left" rowspan="1" colspan="1">160 (86)</td><td align="left" rowspan="1" colspan="1">70 (91)</td><td align="left" rowspan="1" colspan="1">397 (87)</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt101"><label></label><p>*values listed as number (percent of specimens in gender or
age group).</p></fn><fn id="nt102"><label></label><p>**data on sex missing for 25 samples positive for
bacteria, 19 samples positive for parasites, 1 sample positive for
both bacteria and parasites, and 315 samples with no pathogen
identified.</p></fn></table-wrap-foot></table-wrap></sec><sec id="s3b"><title>Epidemiologic review of pathogens</title><p>Overall, 14.4% (644 of 4485) of samples yielded a pathogen. Bacteria
alone were isolated in 8.2% (367 of 4485), parasites alone in
5.6% (253 of 4485) and both parasites and bacteria in 0.5%
(24 of 4485). Of the 367 samples that isolated bacteria alone, 8 samples
isolated two types of pathologic bacteria. Because of this, the total number of
bacterial isolates is 399 (367+24+8). The most common
bacterial pathogens were <italic>Shigella</italic> spp. and
<italic>Salmonella</italic> spp., isolated from 4.0% (180 of 4485)
and 3.9% (175 of 4485) of all specimens, respectively.
<italic>Escherichia coli</italic> (22 of 4485) and
<italic>Campylobacter</italic> spp. (22 of 4485) each accounted for
0.5% of all specimens. Of the <italic>Shigella</italic> spp.,
<italic>S. flexneri</italic> was the most common, accounting for
63.3% (114 of 180) of all <italic>Shigella</italic> isolates,
followed by <italic>S. sonnei</italic> (15.6%), <italic>S.
dysenteriae</italic> (11.1%), and <italic>S. boydii</italic>(7.2%). Data for specific serotypes of <italic>Salmonella</italic>spp. were not available, other than for two cases of <italic>S. typhi</italic>.</p><p>The most common parasites were <italic>Isospora</italic> spp. and
<italic>Cryptosporidium</italic> spp., found in 2.5% (113 of
4485) and 2.2% (99 of 4485) of all specimens, respectively. Other
common parasites were <italic>Giardia lamblia</italic> (0.8%) and
<italic>Taenia</italic> spp. (0.6%).</p><p>Individual pathogens were stratified by patient age and selected study period as
illustrated in <xref ref-type="table" rid="pone-0010924-t002"><bold>Table 2</bold></xref> and <xref ref-type="table" rid="pone-0010924-t003"><bold>Table 3</bold></xref> respectively. The association of WBC or RBC with the presence of
bacterial isolates or parasites is depicted in <xref ref-type="table" rid="pone-0010924-t004"><bold>Table 4</bold></xref>.</p><table-wrap id="pone-0010924-t002" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0010924.t002</object-id><label>Table 2</label><caption><title>Proportion of pathogens by age group<xref ref-type="table-fn" rid="nt104">*</xref>.</title></caption><alternatives><graphic id="pone-0010924-t002-2" xlink:href="pone.0010924.t002"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col></colgroup><thead><tr><td align="left" rowspan="1" colspan="1">Pathogen</td><td colspan="8" align="left" rowspan="1">Age Group [n
(%)]<xref ref-type="table-fn" rid="nt105">**</xref></td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"><1 mo
(n = 95)</td><td align="left" rowspan="1" colspan="1">≥1 mo – <12 mo
(n = 629)</td><td align="left" rowspan="1" colspan="1">≥1 yr – <5 yr
(n = 564)</td><td align="left" rowspan="1" colspan="1">≥5 yr – <15 yr
(n = 313)</td><td align="left" rowspan="1" colspan="1">≥15 yr – <50 yr
(n = 2166)</td><td align="left" rowspan="1" colspan="1">≥50 yr – <65 yr
(n = 185)</td><td align="left" rowspan="1" colspan="1">≥65 yr
(n = 77)</td><td align="left" rowspan="1" colspan="1">Unknown age
(n = 456)</td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">BACTERIA</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Salmonella</italic> spp.</td><td align="left" rowspan="1" colspan="1">1 (1)</td><td align="left" rowspan="1" colspan="1">34 (5)</td><td align="left" rowspan="1" colspan="1">29 (5)</td><td align="left" rowspan="1" colspan="1">13 (4)</td><td align="left" rowspan="1" colspan="1">80 (4)</td><td align="left" rowspan="1" colspan="1">5 (3)</td><td align="left" rowspan="1" colspan="1">2 (3)</td><td align="left" rowspan="1" colspan="1">11 (2)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Escherichia coli</italic></td><td align="left" rowspan="1" colspan="1">2 (2)</td><td align="left" rowspan="1" colspan="1">11 (2)</td><td align="left" rowspan="1" colspan="1">9 (2)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Campylobacter</italic> spp.</td><td align="left" rowspan="1" colspan="1">2 (2)</td><td align="left" rowspan="1" colspan="1">8 (2)</td><td align="left" rowspan="1" colspan="1">8 (1)</td><td align="left" rowspan="1" colspan="1">2 (<1)</td><td align="left" rowspan="1" colspan="1">2 (<1)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Shigella</italic> spp.</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">14 (2)</td><td align="left" rowspan="1" colspan="1">29 (5)</td><td align="left" rowspan="1" colspan="1">16 (5)</td><td align="left" rowspan="1" colspan="1">92 (4)</td><td align="left" rowspan="1" colspan="1">8 (4)</td><td align="left" rowspan="1" colspan="1">3 (4)</td><td align="left" rowspan="1" colspan="1">18 (4)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Total bacterial isolates:</bold></td><td align="left" rowspan="1" colspan="1">5 (5)</td><td align="left" rowspan="1" colspan="1">67 (11)</td><td align="left" rowspan="1" colspan="1">75 (13)</td><td align="left" rowspan="1" colspan="1">31 (10)</td><td align="left" rowspan="1" colspan="1">174 (8)</td><td align="left" rowspan="1" colspan="1">13 (7)</td><td align="left" rowspan="1" colspan="1">5 (6)</td><td align="left" rowspan="1" colspan="1">29 (6)</td></tr><tr><td align="left" rowspan="1" colspan="1">PARASITES</td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Cryptosporidium</italic> spp.</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">25 (4)</td><td align="left" rowspan="1" colspan="1">42 (7)</td><td align="left" rowspan="1" colspan="1">3 (1)</td><td align="left" rowspan="1" colspan="1">17 (<1)</td><td align="left" rowspan="1" colspan="1">7 (4)</td><td align="left" rowspan="1" colspan="1">1 (1)</td><td align="left" rowspan="1" colspan="1">4 (1)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Isospora</italic> spp.</td><td align="left" rowspan="1" colspan="1">1 (1)</td><td align="left" rowspan="1" colspan="1">1 (<1)</td><td align="left" rowspan="1" colspan="1">3 (1)</td><td align="left" rowspan="1" colspan="1">7 (2)</td><td align="left" rowspan="1" colspan="1">78 (4)</td><td align="left" rowspan="1" colspan="1">4 (2)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">19 (4)</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Giardia lamblia</italic></td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">2 (<1)</td><td align="left" rowspan="1" colspan="1">6 (1)</td><td align="left" rowspan="1" colspan="1">7 (2)</td><td align="left" rowspan="1" colspan="1">13 (<1)</td><td align="left" rowspan="1" colspan="1">1 (<1)</td><td align="left" rowspan="1" colspan="1">1 (1)</td><td align="left" rowspan="1" colspan="1">4 (1)</td></tr><tr><td align="left" rowspan="1" colspan="1">Other Parasites</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">1 (<1)</td><td align="left" rowspan="1" colspan="1">4 (1)</td><td align="left" rowspan="1" colspan="1">24 (1)</td><td align="left" rowspan="1" colspan="1">1 (<1)</td><td align="left" rowspan="1" colspan="1">0 (0)</td><td align="left" rowspan="1" colspan="1">3 (<1)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Total parasitic isolates</bold></td><td align="left" rowspan="1" colspan="1">1 (1)</td><td align="left" rowspan="1" colspan="1">28 (4)</td><td align="left" rowspan="1" colspan="1">52 (9)</td><td align="left" rowspan="1" colspan="1">21 (7)</td><td align="left" rowspan="1" colspan="1">132 (6)</td><td align="left" rowspan="1" colspan="1">13 (7)</td><td align="left" rowspan="1" colspan="1">2 (3)</td><td align="left" rowspan="1" colspan="1">30 (7)</td></tr><tr><td align="left" rowspan="1" colspan="1">NO PATHOGEN</td><td align="left" rowspan="1" colspan="1">90 (95)</td><td align="left" rowspan="1" colspan="1">540 (86)</td><td align="left" rowspan="1" colspan="1">448 (79)</td><td align="left" rowspan="1" colspan="1">262 (83)</td><td align="left" rowspan="1" colspan="1">1874 (87)</td><td align="left" rowspan="1" colspan="1">160 (86)</td><td align="left" rowspan="1" colspan="1">70 (91)</td><td align="left" rowspan="1" colspan="1">397 (87)</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt103"><label></label><p>Abbreviations: mo, month(s); yr, year(s); spp, species.</p></fn><fn id="nt104"><label></label><p>*values listed as number (percent of specimens in age
group).</p></fn><fn id="nt105"><label></label><p>**not all columns sum to 100% due to
co-infection with multiple pathogens among some specimens.</p></fn></table-wrap-foot></table-wrap><table-wrap id="pone-0010924-t003" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0010924.t003</object-id><label>Table 3</label><caption><title>Comparison of pathogen proportions between selected study
periods.</title></caption><alternatives><graphic id="pone-0010924-t003-3" xlink:href="pone.0010924.t003"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col></colgroup><thead><tr><td align="left" rowspan="1" colspan="1">Pathogen</td><td align="left" rowspan="1" colspan="1">Feb 2003-Feb 2004 Isolates#
(n = 1332)<xref ref-type="table-fn" rid="nt108">**</xref></td><td align="left" rowspan="1" colspan="1">Jul 2006-Jul 2008 Isolates#
(n = 2845)<xref ref-type="table-fn" rid="nt108">**</xref></td><td align="left" rowspan="1" colspan="1">p-value<xref ref-type="table-fn" rid="nt107">*</xref></td></tr></thead><tbody><tr><td colspan="4" align="left" rowspan="1"><bold>BACTERIA</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Salmonella</italic> spp.</td><td align="left" rowspan="1" colspan="1">48 (4)</td><td align="left" rowspan="1" colspan="1">110 (4)</td><td align="left" rowspan="1" colspan="1">0.728</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Escherichia coli</italic></td><td align="left" rowspan="1" colspan="1">5 (<1)</td><td align="left" rowspan="1" colspan="1">17 (<1)</td><td align="left" rowspan="1" colspan="1">0.492</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Campylobacter</italic> spp.</td><td align="left" rowspan="1" colspan="1">10 (<1)</td><td align="left" rowspan="1" colspan="1">12 (<1)</td><td align="left" rowspan="1" colspan="1">0.175</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Shigella</italic> spp.</td><td align="left" rowspan="1" colspan="1">74 (6)</td><td align="left" rowspan="1" colspan="1">97 (3)</td><td align="left" rowspan="1" colspan="1"><bold>0.001</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Total bacterial isolates:</td><td align="left" rowspan="1" colspan="1">137 (10)</td><td align="left" rowspan="1" colspan="1">236 (8)</td><td align="left" rowspan="1" colspan="1"><bold>0.041</bold></td></tr><tr><td colspan="4" align="left" rowspan="1"><bold>PARASITES</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Cryptosporidium</italic> spp.</td><td align="left" rowspan="1" colspan="1">10 (<1)</td><td align="left" rowspan="1" colspan="1">76 (3)</td><td align="left" rowspan="1" colspan="1"><bold><.001</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Isospora</italic> spp.</td><td align="left" rowspan="1" colspan="1">42 (3)</td><td align="left" rowspan="1" colspan="1">69 (2)</td><td align="left" rowspan="1" colspan="1">0.180</td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Giardia lamblia</italic></td><td align="left" rowspan="1" colspan="1">21 (2)</td><td align="left" rowspan="1" colspan="1">10 (<1)</td><td align="left" rowspan="1" colspan="1"><bold><.001</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Other Parasites</td><td align="left" rowspan="1" colspan="1">5 (<1)</td><td align="left" rowspan="1" colspan="1">25 (1)</td><td align="left" rowspan="1" colspan="1">0.079</td></tr><tr><td align="left" rowspan="1" colspan="1">Total parasitic isolates:</td><td align="left" rowspan="1" colspan="1">78 (6)</td><td align="left" rowspan="1" colspan="1">180 (6)</td><td align="left" rowspan="1" colspan="1">0.582</td></tr><tr><td align="left" rowspan="1" colspan="1">NO PATHOGEN</td><td align="left" rowspan="1" colspan="1">1124 (84)</td><td align="left" rowspan="1" colspan="1">2450 (86)</td><td align="left" rowspan="1" colspan="1">0.143</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt106"><label></label><p># Number (and %) of specimens in selected study
period.</p></fn><fn id="nt107"><label></label><p>*p-values calculated using two-tailed Fisher Exact Test.</p></fn><fn id="nt108"><label></label><p>**not all columns sum to 100% due to
co-infection with multiple pathogens among some specimens.</p></fn></table-wrap-foot></table-wrap><table-wrap id="pone-0010924-t004" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0010924.t004</object-id><label>Table 4</label><caption><title>Association of WBC and RBC with the presence of bacteria or
parasites.</title></caption><alternatives><graphic id="pone-0010924-t004-4" xlink:href="pone.0010924.t004"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col></colgroup><thead><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Bacteria Present</td><td align="left" rowspan="1" colspan="1">Parasites Present</td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><bold>Presence of White Blood Cells</bold></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Sensitivity</td><td align="left" rowspan="1" colspan="1">54.0%</td><td align="left" rowspan="1" colspan="1">30.6%</td></tr><tr><td align="left" rowspan="1" colspan="1">Specificity</td><td align="left" rowspan="1" colspan="1">74.2%</td><td align="left" rowspan="1" colspan="1">69.9%</td></tr><tr><td align="left" rowspan="1" colspan="1">Positive Predictive Value</td><td align="left" rowspan="1" colspan="1">27.4%</td><td align="left" rowspan="1" colspan="1">10.8%</td></tr><tr><td align="left" rowspan="1" colspan="1">Negative Predictive Value</td><td align="left" rowspan="1" colspan="1">90.0%</td><td align="left" rowspan="1" colspan="1">89.4%</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Presence of Red Blood Cells</bold></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Sensitivity</td><td align="left" rowspan="1" colspan="1">21.4%</td><td align="left" rowspan="1" colspan="1">3.7%</td></tr><tr><td align="left" rowspan="1" colspan="1">Specificity</td><td align="left" rowspan="1" colspan="1">92.2%</td><td align="left" rowspan="1" colspan="1">89.4%</td></tr><tr><td align="left" rowspan="1" colspan="1">Positive Predictive Value</td><td align="left" rowspan="1" colspan="1">33.2%</td><td align="left" rowspan="1" colspan="1">4.0%</td></tr><tr><td align="left" rowspan="1" colspan="1">Negative Predictive Value</td><td align="left" rowspan="1" colspan="1">86.7%</td><td align="left" rowspan="1" colspan="1">88.6%</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Presence of Both White and Red Blood Cells</bold></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Sensitivity</td><td align="left" rowspan="1" colspan="1">21.5%</td><td align="left" rowspan="1" colspan="1">3.7%</td></tr><tr><td align="left" rowspan="1" colspan="1">Specificity</td><td align="left" rowspan="1" colspan="1">92.9%</td><td align="left" rowspan="1" colspan="1">90.1%</td></tr><tr><td align="left" rowspan="1" colspan="1">Positive Predictive Value</td><td align="left" rowspan="1" colspan="1">35.2%</td><td align="left" rowspan="1" colspan="1">4.3%</td></tr><tr><td align="left" rowspan="1" colspan="1">Negative Predictive Value</td><td align="left" rowspan="1" colspan="1">86.9%</td><td align="left" rowspan="1" colspan="1">88.7%</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt109"><label></label><p>Abbreviations: WBC, white blood cells; RBC, red blood cells; WBC or
RBC were counted as present if laboratory records indicated scanty,
few, moderate, or many cells upon microscopic evaluation.</p></fn></table-wrap-foot></table-wrap></sec><sec id="s3c"><title>Antimicrobial Susceptibility</title><p>Susceptibility data were available for 87.7% (350 of 399) of positive
bacterial isolates. Because data were most consistently available for
susceptibility to ampicillin, trimethoprim-sulfamethoxazole, chloramphenicol,
and nalidixic acid within the two selected study periods, resistance patterns to
these antimicrobials for all bacterial isolates were compared (<xref ref-type="table" rid="pone-0010924-t005"><bold>Table 5</bold></xref>). There was a significant increase in resistance to ampicillin among
<italic>Shigella</italic> spp. isolates and a significant decrease in
resistance to chloramphenicol among <italic>Salmonella</italic> spp. isolates
over time. No <italic>Salmonella</italic> spp. or <italic>Shigella</italic> spp.
isolates were resistant to ciprofloxacin, while 0% (0 of 10) and
22% (2 of 9) <italic>Campylobacter</italic> spp. were resistant to
ciprofloxacin in the earlier and later selected study periods, respectively.
When all bacterial isolates were pooled together, significant findings were an
increase in ampicillin resistance (p<0.001), and decreased resistance to
trimethoprim-sulfamethoxazole (p = 0.028) and
chloramphenicol (p = 0.001).</p><table-wrap id="pone-0010924-t005" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0010924.t005</object-id><label>Table 5</label><caption><title>Comparison of antibiotic resistance among <italic>Salmonella</italic>spp., <italic>Shigella</italic> spp., and all bacterial
isolates.</title></caption><alternatives><graphic id="pone-0010924-t005-5" xlink:href="pone.0010924.t005"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col></colgroup><thead><tr><td align="left" rowspan="1" colspan="1">Antibiotic</td><td align="left" rowspan="1" colspan="1">Feb 2003-Feb 2004 Resistant Isolates#</td><td align="left" rowspan="1" colspan="1">Jul 2006-Jul 2008 Resistant Isolates#</td><td align="left" rowspan="1" colspan="1">p-value<xref ref-type="table-fn" rid="nt111">*</xref></td></tr></thead><tbody><tr><td colspan="4" align="left" rowspan="1"><bold><italic>Salmonella</italic></bold><bold> spp.</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Ampicillin</td><td align="left" rowspan="1" colspan="1">19/46 (41)</td><td align="left" rowspan="1" colspan="1">43/87 (49)</td><td align="left" rowspan="1" colspan="1">0.465</td></tr><tr><td align="left" rowspan="1" colspan="1">Trimethoprim-Sulfamethoxazole</td><td align="left" rowspan="1" colspan="1">16/46 (35)</td><td align="left" rowspan="1" colspan="1">19/86 (22)</td><td align="left" rowspan="1" colspan="1">0.148</td></tr><tr><td align="left" rowspan="1" colspan="1">Chloramphenicol</td><td align="left" rowspan="1" colspan="1">14/25 (56)</td><td align="left" rowspan="1" colspan="1">5/82 (6)</td><td align="left" rowspan="1" colspan="1"><bold><.001</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Nalidixic Acid</td><td align="left" rowspan="1" colspan="1">4/25 (16)</td><td align="left" rowspan="1" colspan="1">22/87 (25)</td><td align="left" rowspan="1" colspan="1">0.426</td></tr><tr><td colspan="4" align="left" rowspan="1"><bold><italic>Shigella</italic></bold><bold> spp.</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Ampicillin</td><td align="left" rowspan="1" colspan="1">32/74 (43)</td><td align="left" rowspan="1" colspan="1">66/80 (83)</td><td align="left" rowspan="1" colspan="1"><bold><.001</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Trimethoprim-Sulfamethoxazole</td><td align="left" rowspan="1" colspan="1">60/74 (81)</td><td align="left" rowspan="1" colspan="1">62/80 (78)</td><td align="left" rowspan="1" colspan="1">0.692</td></tr><tr><td align="left" rowspan="1" colspan="1">Chloramphenicol</td><td align="left" rowspan="1" colspan="1">6/16 (38)</td><td align="left" rowspan="1" colspan="1">21/79 (27)</td><td align="left" rowspan="1" colspan="1">0.378</td></tr><tr><td align="left" rowspan="1" colspan="1">Nalidixic Acid</td><td align="left" rowspan="1" colspan="1">0/16 (0)</td><td align="left" rowspan="1" colspan="1">8/80 (10)</td><td align="left" rowspan="1" colspan="1">0.345</td></tr><tr><td colspan="4" align="left" rowspan="1"><bold>All Bacterial Isolates (</bold><bold><italic>Salmonella, Shigella</italic></bold><bold>, </bold><bold><italic>Campylobacter</italic></bold><bold>, </bold><bold><italic>E. coli</italic></bold><bold>)</bold><xref ref-type="table-fn" rid="nt112">†</xref></td></tr><tr><td align="left" rowspan="1" colspan="1">Ampicillin</td><td align="left" rowspan="1" colspan="1">56/127 (44)</td><td align="left" rowspan="1" colspan="1">125/189 (66)</td><td align="left" rowspan="1" colspan="1"><bold><.001</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Trimethoprim-Sulfamethoxazole</td><td align="left" rowspan="1" colspan="1">82/127 (65)</td><td align="left" rowspan="1" colspan="1">97/187 (52)</td><td align="left" rowspan="1" colspan="1"><bold>0.028</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Chloramphenicol</td><td align="left" rowspan="1" colspan="1">21/51 (41)</td><td align="left" rowspan="1" colspan="1">31/182 (17)</td><td align="left" rowspan="1" colspan="1"><bold>0.001</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Nalidixic Acid</td><td align="left" rowspan="1" colspan="1">6/43 (14)</td><td align="left" rowspan="1" colspan="1">37/189 (20)</td><td align="left" rowspan="1" colspan="1">0.515</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt110"><label></label><p># Number (and %) of organisms resistant.</p></fn><fn id="nt111"><label></label><p>*p-values calculated using two-tailed Fisher Exact Test.</p></fn><fn id="nt112"><label></label><p>†This section includes all bacterial isolates
(<italic>Salmonella spp.</italic>and <italic>Shigella
spp.</italic>as well as the few isolates of <italic>Campylobacter
spp.</italic> and <italic>E.coli</italic>). This summary section
may be a useful guide to empiric therapy of dysentery in Southern
Botswana.</p></fn></table-wrap-foot></table-wrap><p>Of 644 specimens that yielded a pathogenic organism, data regarding previous
antimicrobial exposure within two weeks of specimen collection were available
for 22% (139 of 644). Of these, 24% (33 of 139) were
exposed to antimicrobials within 2 weeks as follows: cefotaxime 33%
(11 of 33), trimethoprim-sulfamethoxazole 30% (10 of 33), and
metronidazole 24% (8 of 33).</p></sec></sec><sec id="s4"><title>Discussion</title><p>Our study reports a high proportion of stool specimens with no identifiable
pathogenic bacteria or parasites. When pathogens were identified,
<italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp. were the most
common bacteria, while <italic>Isospora</italic> spp. and
<italic>Cryptosporidium</italic> spp. were the most common parasites. We also
identified important trends in antimicrobial susceptibility among common agents
responsible for gastroenteritis in southern Africa. The proportion of resistance to
ampicillin and trimethoprim-sulfamethoxazole among common pathogens was high,
supporting the utility of nalidixic acid as empiric therapy for suspected bacterial
dysenteric gastroenteritis. Although significant changes in resistance to nalidixic
acid were absent, susceptibility to this agent should be closely monitored.</p><p>Compared with previous studies of diarrheal disease in the region, our data showed a
markedly lower overall proportion of bacterial and parasitic isolates. These
differences could be partially attributed to the fact that few other regional
studies comprehensively evaluated a similar breadth of pathogens, and most were
restricted to children. In our study, if we restricted the proportion analysis of
bacterial pathogens to children younger than 5 years of age, the rate increases to
11.1% (143 of 1288), although this is still lower than other regional
studies. Studies from Zimbabwe, Mozambique, South Africa, and Kenya have reported
bacterial pathogens in 22% to 32% of specimens from patients
with diarrheal disease <xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>, <xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>, <xref ref-type="bibr" rid="pone.0010924-Lin1">[16]</xref>, <xref ref-type="bibr" rid="pone.0010924-Simango1">[17]</xref>. The
same studies from Mozambique and South Africa also reported that 11 to
14% of specimens contained a parasite <xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>, <xref ref-type="bibr" rid="pone.0010924-Lin1">[16]</xref>. In our
study, parasite proportion analysis restricted to children under 5 years of age
showed an increased, although still discordant, number of 6.3% (67 of
1288) of specimens contained a parasite.</p><p>The proportion of specimens positive for <italic>Shigella</italic> spp. was also
substantially lower than most other estimates in the region, which ranged from
10–16% <xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>, <xref ref-type="bibr" rid="pone.0010924-Temu1">[12]</xref>, <xref ref-type="bibr" rid="pone.0010924-Simango1">[17]</xref>, <xref ref-type="bibr" rid="pone.0010924-Nakano1">[18]</xref>, <xref ref-type="bibr" rid="pone.0010924-Simango2">[19]</xref>. However, a study in
southern Mozambique of children <5 years with diarrheal disease indicated a
lower proportion of <italic>Shigella</italic> spp. of 0.2% <xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>. The
antimicrobial susceptibilities we describe for <italic>Shigella</italic> isolates
are similar to those previously reported from the region with ranges of resistance
reported at 77–97% for ampicillin, 90–97%
for trimethoprim-sulfamethoxazole, 27–88% for chloramphenicol,
0–3% for ciprofloxacin, and 0–2% for
nalidixic acid <xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>, <xref ref-type="bibr" rid="pone.0010924-Mwansa1">[9]</xref>, <xref ref-type="bibr" rid="pone.0010924-Temu1">[12]</xref>.</p><p>In the present study, the proportion of <italic>Salmonella</italic> spp. was similar
to other estimates from the region, which ranged from 1.4–5.8%
<xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>, <xref ref-type="bibr" rid="pone.0010924-Simango1">[17]</xref>, <xref ref-type="bibr" rid="pone.0010924-Nakano1">[18]</xref>, <xref ref-type="bibr" rid="pone.0010924-Simango2">[19]</xref>. In addition, the
percent of resistance among <italic>Salmonella</italic> isolates was similar to
regional studies with ranges of 13–62% for ampicillin,
4–88% for trimethoprim-sulfamethoxazole,
3–36% for chloramphenicol, 0–1% for
ciprofloxacin and 3–33% for nalidixic acid) <xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>, <xref ref-type="bibr" rid="pone.0010924-Mwansa1">[9]</xref>, <xref ref-type="bibr" rid="pone.0010924-Temu1">[12]</xref>, <xref ref-type="bibr" rid="pone.0010924-Simango1">[17]</xref>.</p><p>We also reported a lower overall proportion of <italic>Campylobacter</italic> spp.,
<italic>E. coli</italic>, <italic>Isospora</italic> spp.,
<italic>Cryptosporidium</italic> spp., and <italic>G. lamblia</italic>, than
have been seen in other studies in the region. For these pathogens, other
Sub-Saharan Africa studies have indicated ranges of: <italic>Campylobacter</italic>spp. (1–9%), <italic>E. coli</italic>(2–23%), <italic>Isospora</italic>spp.(12%), <italic>Cryptosporidium</italic> spp.
(0.5–16%), and <italic>G. lamblia</italic>(1–7%) <xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>, <xref ref-type="bibr" rid="pone.0010924-Cranendonk1">[6]</xref>, <xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Lin1">[16]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Simango1">[17]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Nakano1">[18]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Simango2">[19]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Gumbo1">[20]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Luo1">[21]</xref>,
<xref ref-type="bibr" rid="pone.0010924-Morse1">[22]</xref>.</p><p>The calculated sensitivity, specificity, positive predictive value, and negative
predictive value of WBC and/or RBC in determining the presence of bacteria were
within reported ranges of previous studies examining acute infectious diarrhea <xref ref-type="bibr" rid="pone.0010924-Huicho1">[23]</xref>. In
this setting, the absence of WBC and/or RBC was generally correlated with a high
specificity and negative predictive value for the absence of bacteria or parasites.</p><p>The only similar study concerning diarrheal disease in Gaborone included 221 children
with diarrhea enrolled prospectively from July through November, 1998 at a single
clinic serving a relatively socioeconomically poor area <xref ref-type="bibr" rid="pone.0010924-Urio1">[24]</xref>. The 21%
prevalence of <italic>Shigella</italic> spp. in that study was higher than the
present study (4.0% of all samples); 89% of isolates were
resistant to ampicillin and 39% were resistant to
trimethoprim-sulfamethoxazole. The prevalence of <italic>Salmonella</italic> spp.,
was similar to that found in our study and, in contrast to our results, all
<italic>Salmonella</italic> spp. were sensitive to ampicillin and
trimethoprim-sulfamethoxazole. While prospective, the <italic>Urio et al</italic>study was limited to a five month period, did not examine antimicrobial resistance
in enteropathogens other than <italic>Salmonella</italic> or
<italic>Shigella</italic> and reflects a single clinic pediatric experience in a low
socioeconomic setting <xref ref-type="bibr" rid="pone.0010924-Urio1">[24]</xref>.</p><p>There are several possible explanations for the discrepancy in enteropathogen
prevalence rates between this study and others previously discussed. The majority of
specimens in this study are from outpatient clinics, while many previous studies
were restricted to inpatient admissions. Inpatient samples may select for more
severe cases of diarrhea and thus bias those studies toward a higher prevalence of
bacterial pathogens <xref ref-type="bibr" rid="pone.0010924-Mandomando1">[8]</xref>, <xref ref-type="bibr" rid="pone.0010924-Lin1">[16]</xref>. Because of the retrospective design, we could
not control for the amount of time between specimen collection and analysis; this
may have biased our results towards a larger proportion of samples being negative
for bacteria and/or parasites, as some bacteria (e.g. <italic>Shigella,
Campylobacter</italic>) and many parasites are sensitive to desiccation when
left in the specimen container for an extended period of time. This bias would cause
us to underestimate the prevalence of some pathogens, but would not impact the
interpretation of susceptibility data. Because Botswana has one of the highest HIV
prevalence rates in Africa <xref ref-type="bibr" rid="pone.0010924-Organization1">[13]</xref>, there may also be a larger proportion of
negative specimens due to a relatively higher prevalence of HIV enteropathy. Some
regional variation in pathogen prevalence is also expected, as climate, seasonality,
and socioeconomic conditions are influential. In addition, the water supply and
sanitation in the study area are relatively good. This makes contamination of
drinking water by bacteria or parasites less likely thereby decreasing their
proportional contribution as a cause of gastroenteritis.</p><p>This study had several limitations. Our retrospective and descriptive design makes
our results susceptible to all limitations and potential biases of studies of
similar design. We were unable to account for multiple specimens from the same
patient, which precluded incidence rate calculation. Data on recent antimicrobial
exposure were not routinely available, although those samples for which data were
available indicated that the percentage of specimens previously exposed to
antimicrobials was relatively low. Due to the retrospective study design, standard
laboratory techniques and data recording practices shifted over the course of the
study period. Because of changes in laboratory practices, isolates of
<italic>Salmonella</italic> and <italic>Shigella</italic> were submitted to
different susceptibility testing panels before and after October 2003. It has also
been laboratory practice not to routinely differentiate <italic>Cyclospora</italic>from <italic>Cryptosporidium</italic>; thus, the prevalence of
<italic>Cryptosporidium</italic> may be lower than reported in this study.
However, there have been few reported cases of <italic>Cyclospora</italic> in
Sub-Saharan Africa, and we believe this contribution to be negligible <xref ref-type="bibr" rid="pone.0010924-Gumbo1">[20]</xref>, <xref ref-type="bibr" rid="pone.0010924-Karanja1">[25]</xref>. We
were unable to obtain the HIV status of patients from whom stool specimens were
submitted. HIV itself may predispose our patient population to specific pathogens in
this HIV endemic region and thus limit the generalizability of our data. Our study
does, however, encompass a longer time period and larger sample size than other
reports from the region <xref ref-type="bibr" rid="pone.0010924-Brooks1">[5]</xref>. Additionally, we describe antimicrobial
resistance patterns over time and, by including both inpatient and outpatient
specimens from a wide variety of centers, we limited the referral bias likely
present in other studies that examined only inpatients with diarrhea. Both of these
aspects are novel for data from the southern African region.</p><p>In summary, this study demonstrates a high prevalence of samples negative for
bacteria and parasites, likely indicating a high prevalence of viral illness
although further prospective studies are needed to confirm such findings.
<italic>Shigella</italic> spp. and <italic>Salmonella</italic> spp. were the
most common bacteria; <italic>Isospora</italic> spp. and
<italic>Cryptosporidium</italic> spp. were the most common parasites. Resistance to
commonly used antimicrobials among enteropathogens in Gaborone, Botswana and the
surrounding area is high. Nalidixic acid may provide the best alternative for
empiric therapy in a patient with dysentery, although such use should be closely
monitored as resistance to nalidixic acid is also increasing.</p></sec></body><back><fn-group><fn fn-type="conflict"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="financial-disclosure"><p><bold>Funding: </bold>Supported in part by the University of Pennsylvania Center for AIDS Research
IP30AI45008-01 to APS (<ext-link ext-link-type="uri" xlink:href="http://www.uphs.upenn.edu/aids/">http://www.uphs.upenn.edu/aids/</ext-link>), Infectious Diseases Society of
America Medical Student Award & UPenn Center for Clinical Epidemiology
and Biostatistics Medical Student Award to JSR (<ext-link ext-link-type="uri" xlink:href="http://www.idsociety.org/Content.aspx?id=1852">http://www.idsociety.org/Content.aspx?id=1852</ext-link>). SSS was
supported by the Robert Wood Johnson Foundation through its Physician Faculty
Scholar Program (<ext-link ext-link-type="uri" xlink:href="http://rwjfpfsp.stanford.edu/">http://rwjfpfsp.stanford.edu/</ext-link>). The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the
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