Diabetic Peripheral Neuropathy in Ambulatory Patients with Type 2 Diabetes in a General Hospital in a Middle Income Country: A Cross-Sectional Study
Identifieur interne : 000751 ( Pmc/Corpus ); précédent : 000750; suivant : 000752Diabetic Peripheral Neuropathy in Ambulatory Patients with Type 2 Diabetes in a General Hospital in a Middle Income Country: A Cross-Sectional Study
Auteurs : María De Los Angeles Lazo ; Antonio Bernabé-Ortiz ; Miguel E. Pinto ; Ray Ticse ; German Malaga ; Katherine Sacksteder ; J. Jaime Miranda ; Robert H. GilmanSource :
- PLoS ONE [ 1932-6203 ] ; 2014.
Abstract
We aimed to estimate the morbidity rate and associated factors for diabetic peripheral neuropathy (DPN) in a low-middle income country setting.
Cross-sectional study, data was gathered at Peru's Ministry of Health national specialized hospital for endocrinological conditions through standardized interviews, anthropometric measurements and blood tests for glycated haemoglobin (HbA1c). DPN was evaluated using two techniques: the Semmes-Weinstein monofilament test and the diabetic neuropathy symptom score. Overall prevalence and 95% confidence intervals (95% CI) were calculated. Potential factors related to DPN explored included body mass index, years with disease (<10 vs. ≥10 years), glycaemic control (HbA1c <7% vs. ≥7%), microalbuminuria, retinopathy, and current pharmacological treatment. Multivariable analysis was performed using Poisson analysis to calculate prevalence ratios.
DPN was observed in 73/129 (56.6%) patients. In multivariable analysis adjusted by age and sex, the prevalence ratio of neuropathy was 1.4 times higher (95% CI 1.07–1.88) in patients who took insulin plus metformin compared to patients who used one treatment alone, and 1.4 higher (95% CI 1.02–1.93) in patients with ≥10 years of disease compared to those with a shorter duration of disease. Also we found some characteristics in foot evaluation associated to neuropathy such as deformities (p<0.001), onychomycosis (p = 0.012), abnormal Achilles reflex (p<0.001), pain perception (p<0.001) and vibration perception (p<0.001).
DPN is highly frequent among patients with diabetes in a national specialized facility from Peru. Associated factors to DPN included being a diabetic patient for over ten years, and receiving insulin plus metformin
Url:
DOI: 10.1371/journal.pone.0095403
PubMed: 24789071
PubMed Central: 4006783
Links to Exploration step
PMC:4006783Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Diabetic Peripheral Neuropathy in Ambulatory Patients with Type 2 Diabetes in a General Hospital in a Middle Income Country: A Cross-Sectional Study</title><author><name sortKey="Lazo, Maria De Los Angeles" sort="Lazo, Maria De Los Angeles" uniqKey="Lazo M" first="María De Los Angeles" last="Lazo">María De Los Angeles Lazo</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>Unidad de Conocimiento y Evidencia, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Bernabe Ortiz, Antonio" sort="Bernabe Ortiz, Antonio" uniqKey="Bernabe Ortiz A" first="Antonio" last="Bernabé-Ortiz">Antonio Bernabé-Ortiz</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Pinto, Miguel E" sort="Pinto, Miguel E" uniqKey="Pinto M" first="Miguel E." last="Pinto">Miguel E. Pinto</name><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Servicio de Endocrinología, Hospital Nacional Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ticse, Ray" sort="Ticse, Ray" uniqKey="Ticse R" first="Ray" last="Ticse">Ray Ticse</name><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Servicio de Endocrinología, Hospital Nacional Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Malaga, German" sort="Malaga, German" uniqKey="Malaga G" first="German" last="Malaga">German Malaga</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>Unidad de Conocimiento y Evidencia, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Sacksteder, Katherine" sort="Sacksteder, Katherine" uniqKey="Sacksteder K" first="Katherine" last="Sacksteder">Katherine Sacksteder</name><affiliation><nlm:aff id="aff5"><addr-line>Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Miranda, J Jaime" sort="Miranda, J Jaime" uniqKey="Miranda J" first="J. Jaime" last="Miranda">J. Jaime Miranda</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Gilman, Robert H" sort="Gilman, Robert H" uniqKey="Gilman R" first="Robert H." last="Gilman">Robert H. Gilman</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><addr-line>Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America</addr-line></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24789071</idno><idno type="pmc">4006783</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4006783</idno><idno type="RBID">PMC:4006783</idno><idno type="doi">10.1371/journal.pone.0095403</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000751</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000751</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Diabetic Peripheral Neuropathy in Ambulatory Patients with Type 2 Diabetes in a General Hospital in a Middle Income Country: A Cross-Sectional Study</title><author><name sortKey="Lazo, Maria De Los Angeles" sort="Lazo, Maria De Los Angeles" uniqKey="Lazo M" first="María De Los Angeles" last="Lazo">María De Los Angeles Lazo</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>Unidad de Conocimiento y Evidencia, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Bernabe Ortiz, Antonio" sort="Bernabe Ortiz, Antonio" uniqKey="Bernabe Ortiz A" first="Antonio" last="Bernabé-Ortiz">Antonio Bernabé-Ortiz</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Pinto, Miguel E" sort="Pinto, Miguel E" uniqKey="Pinto M" first="Miguel E." last="Pinto">Miguel E. Pinto</name><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Servicio de Endocrinología, Hospital Nacional Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Ticse, Ray" sort="Ticse, Ray" uniqKey="Ticse R" first="Ray" last="Ticse">Ray Ticse</name><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><addr-line>Servicio de Endocrinología, Hospital Nacional Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Malaga, German" sort="Malaga, German" uniqKey="Malaga G" first="German" last="Malaga">German Malaga</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><addr-line>Unidad de Conocimiento y Evidencia, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Sacksteder, Katherine" sort="Sacksteder, Katherine" uniqKey="Sacksteder K" first="Katherine" last="Sacksteder">Katherine Sacksteder</name><affiliation><nlm:aff id="aff5"><addr-line>Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America</addr-line></nlm:aff></affiliation></author><author><name sortKey="Miranda, J Jaime" sort="Miranda, J Jaime" uniqKey="Miranda J" first="J. Jaime" last="Miranda">J. Jaime Miranda</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation></author><author><name sortKey="Gilman, Robert H" sort="Gilman, Robert H" uniqKey="Gilman R" first="Robert H." last="Gilman">Robert H. Gilman</name><affiliation><nlm:aff id="aff1"><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><addr-line>Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, 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="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Aim</title><p>We aimed to estimate the morbidity rate and associated factors for diabetic peripheral neuropathy (DPN) in a low-middle income country setting.</p></sec><sec><title>Methods</title><p>Cross-sectional study, data was gathered at Peru's Ministry of Health national specialized hospital for endocrinological conditions through standardized interviews, anthropometric measurements and blood tests for glycated haemoglobin (HbA1c). DPN was evaluated using two techniques: the Semmes-Weinstein monofilament test and the diabetic neuropathy symptom score. Overall prevalence and 95% confidence intervals (95% CI) were calculated. Potential factors related to DPN explored included body mass index, years with disease (<10 vs. ≥10 years), glycaemic control (HbA1c <7% vs. ≥7%), microalbuminuria, retinopathy, and current pharmacological treatment. Multivariable analysis was performed using Poisson analysis to calculate prevalence ratios.</p></sec><sec><title>Results</title><p>DPN was observed in 73/129 (56.6%) patients. In multivariable analysis adjusted by age and sex, the prevalence ratio of neuropathy was 1.4 times higher (95% CI 1.07–1.88) in patients who took insulin plus metformin compared to patients who used one treatment alone, and 1.4 higher (95% CI 1.02–1.93) in patients with ≥10 years of disease compared to those with a shorter duration of disease. Also we found some characteristics in foot evaluation associated to neuropathy such as deformities (p<0.001), onychomycosis (p = 0.012), abnormal Achilles reflex (p<0.001), pain perception (p<0.001) and vibration perception (p<0.001).</p></sec><sec><title>Conclusion</title><p>DPN is highly frequent among patients with diabetes in a national specialized facility from Peru. Associated factors to DPN included being a diabetic patient for over ten years, and receiving insulin plus metformin</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Chan, Jc" uniqKey="Chan J">JC Chan</name></author><author><name sortKey="Gagliardino, Jj" uniqKey="Gagliardino J">JJ Gagliardino</name></author><author><name sortKey="Baik, Sh" uniqKey="Baik S">SH Baik</name></author><author><name sortKey="Chantelot, Jm" uniqKey="Chantelot J">JM Chantelot</name></author><author><name sortKey="Ferreira, Sr" uniqKey="Ferreira S">SR Ferreira</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tres, Gs" uniqKey="Tres G">GS Tres</name></author><author><name sortKey="Lisboa, Hr" uniqKey="Lisboa H">HR Lisbôa</name></author><author><name sortKey="Syllos, R" uniqKey="Syllos R">R Syllos</name></author><author><name sortKey="Canani, Lh" uniqKey="Canani L">LH Canani</name></author><author><name sortKey="Gross, Jl" uniqKey="Gross J">JL Gross</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bos, M" uniqKey="Bos M">M Bos</name></author><author><name sortKey="Agyemang, C" uniqKey="Agyemang C">C Agyemang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Singh, N" uniqKey="Singh N">N Singh</name></author><author><name sortKey="Armstrong, Dg" uniqKey="Armstrong D">DG Armstrong</name></author><author><name sortKey="Lipsky, Ba" uniqKey="Lipsky B">BA Lipsky</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Tentolouris, N" uniqKey="Tentolouris N">N Tentolouris</name></author><author><name sortKey="Al Sabbagh, S" uniqKey="Al Sabbagh S">S Al-Sabbagh</name></author><author><name sortKey="Walker, Mg" uniqKey="Walker M">MG Walker</name></author><author><name sortKey="Boulton, Aj" uniqKey="Boulton A">AJ Boulton</name></author><author><name sortKey="Jude, Eb" uniqKey="Jude E">EB Jude</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ollendorf, Da" uniqKey="Ollendorf D">DA Ollendorf</name></author><author><name sortKey="Kotsanos, Jg" uniqKey="Kotsanos J">JG Kotsanos</name></author><author><name sortKey="Wishner, Wj" uniqKey="Wishner W">WJ Wishner</name></author><author><name sortKey="Friedman, M" uniqKey="Friedman M">M Friedman</name></author><author><name sortKey="Cooper, T" uniqKey="Cooper T">T Cooper</name></author><author><name sortKey="Bittoni, M" uniqKey="Bittoni M">M Bittoni</name></author><author><name sortKey="Oster, G" uniqKey="Oster G">G Oster</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Boulton, Aj" uniqKey="Boulton A">AJ Boulton</name></author><author><name sortKey="Armstrong, Dg" uniqKey="Armstrong D">DG Armstrong</name></author><author><name sortKey="Albert, Sf" uniqKey="Albert S">SF Albert</name></author><author><name sortKey="Frykberg, Rg" uniqKey="Frykberg R">RG Frykberg</name></author><author><name sortKey="Hellman, R" uniqKey="Hellman R">R Hellman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mcneely, Mj" uniqKey="Mcneely M">MJ McNeely</name></author><author><name sortKey="Boyko, E" uniqKey="Boyko E">E Boyko</name></author><author><name sortKey="Ahroni, Jh" uniqKey="Ahroni J">JH Ahroni</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Meijer, Jw" uniqKey="Meijer J">JW Meijer</name></author><author><name sortKey="Smit, Aj" uniqKey="Smit A">AJ Smit</name></author><author><name sortKey="Sonderen, Ev" uniqKey="Sonderen E">EV Sonderen</name></author><author><name sortKey="Groothoff, Jw" uniqKey="Groothoff J">JW Groothoff</name></author><author><name sortKey="Eisma, Wh" uniqKey="Eisma W">WH Eisma</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Menchaca Diaz, R" uniqKey="Menchaca Diaz R">R Menchaca-Díaz</name></author><author><name sortKey="Bogarin L Pez, B" uniqKey="Bogarin L Pez B">B Bogarín-López</name></author><author><name sortKey="Zamudio G Mez, Ma" uniqKey="Zamudio G Mez M">MA Zamudio-Gómez</name></author><author><name sortKey="Anzaldo Campos, Mc" uniqKey="Anzaldo Campos M">MC Anzaldo-Campos</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Karvestedt, L" uniqKey="Karvestedt L">L Karvestedt</name></author><author><name sortKey="Martensson, E" uniqKey="Martensson E">E Martensson</name></author><author><name sortKey="Grill, V" uniqKey="Grill V">V Grill</name></author><author><name sortKey="Elofsson, S" uniqKey="Elofsson S">S Elofsson</name></author><author><name sortKey="Von Wendt, G" uniqKey="Von Wendt G">G von Wendt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ko, Sh" uniqKey="Ko S">SH Ko</name></author><author><name sortKey="Cha, By" uniqKey="Cha B">BY Cha</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Janghorbani, M" uniqKey="Janghorbani M">M Janghorbani</name></author><author><name sortKey="Rezvanian, H" uniqKey="Rezvanian H">H Rezvanian</name></author><author><name sortKey="Kachooei, A" uniqKey="Kachooei A">A Kachooei</name></author><author><name sortKey="Ghorbani, A" uniqKey="Ghorbani A">A Ghorbani</name></author><author><name sortKey="Chitsaz, A" uniqKey="Chitsaz A">A Chitsaz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ibarra, Ct" uniqKey="Ibarra C">CT Ibarra</name></author><author><name sortKey="Rocha Jde, J" uniqKey="Rocha Jde J">J Rocha Jde</name></author><author><name sortKey="Hernandez, Ro" uniqKey="Hernandez R">RO Hernández</name></author><author><name sortKey="Nieves, Re" uniqKey="Nieves R">RE Nieves</name></author><author><name sortKey="Leyva, Rj" uniqKey="Leyva R">RJ Leyva</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Mold, Jw" uniqKey="Mold J">JW Mold</name></author><author><name sortKey="Vesely, Sk" uniqKey="Vesely S">SK Vesely</name></author><author><name sortKey="Keyl, Ba" uniqKey="Keyl B">BA Keyl</name></author><author><name sortKey="Schenk, Jb" uniqKey="Schenk J">JB Schenk</name></author><author><name sortKey="Roberts, M" uniqKey="Roberts M">M Roberts</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Currie, Cj" uniqKey="Currie C">CJ Currie</name></author><author><name sortKey="Poole, Cd" uniqKey="Poole C">CD Poole</name></author><author><name sortKey="Evans, M" uniqKey="Evans M">M Evans</name></author><author><name sortKey="Peters, Jr" uniqKey="Peters J">JR Peters</name></author><author><name sortKey="Morgan, Cl" uniqKey="Morgan C">CL Morgan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chung, Jo" uniqKey="Chung J">JO Chung</name></author><author><name sortKey="Cho, Dh" uniqKey="Cho D">DH Cho</name></author><author><name sortKey="Chung, Dj" uniqKey="Chung D">DJ Chung</name></author><author><name sortKey="Chung, My" uniqKey="Chung M">MY Chung</name></author></analytic></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">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">24789071</article-id><article-id pub-id-type="pmc">4006783</article-id><article-id pub-id-type="publisher-id">PONE-D-14-04554</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0095403</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine and Health Sciences</subject><subj-group><subject>Endocrinology</subject><subj-group><subject>Diabetic Endocrinology</subject></subj-group></subj-group><subj-group><subject>Epidemiology</subject><subj-group><subject>Clinical Epidemiology</subject></subj-group></subj-group><subj-group><subject>Metabolic Disorders</subject><subj-group><subject>Diabetes Mellitus</subject><subj-group><subject>Type 2 Diabetes</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Diabetic Peripheral Neuropathy in Ambulatory Patients with Type 2 Diabetes in a General Hospital in a Middle Income Country: A Cross-Sectional Study</article-title><alt-title alt-title-type="running-head">Diabetic Peripheral Neuropathy in Ambulatory Patients of a LMIC</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Lazo</surname><given-names>María de los Angeles</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>Bernabé-Ortiz</surname><given-names>Antonio</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Pinto</surname><given-names>Miguel E.</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>Ticse</surname><given-names>Ray</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>Malaga</surname><given-names>German</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="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sacksteder</surname><given-names>Katherine</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Miranda</surname><given-names>J. Jaime</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gilman</surname><given-names>Robert H.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>CRONICAS Centre of Excellence in Chronic Diseases, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Unidad de Conocimiento y Evidencia, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Facultad de Medicina “Alberto Hurtado”, Universidad Peruana Cayetano Heredia, Lima, Peru</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Servicio de Endocrinología, Hospital Nacional Cayetano Heredia, Lima, Peru</addr-line></aff><aff id="aff5"><label>5</label><addr-line>Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>James</surname><given-names>Leighton R.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University of Florida, United States of America</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>Jaime.Miranda@upch.pe</email></corresp><fn fn-type="conflict"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: JJM RHG. Performed the experiments: MP RT. Analyzed the data: ML ABO JJM. Contributed reagents/materials/analysis tools: ABO. Wrote the paper: ML ABO GM KS JJM RHG.</p></fn></author-notes><pub-date pub-type="collection"><year>2014</year></pub-date><pub-date pub-type="epub"><day>1</day><month>5</month><year>2014</year></pub-date><volume>9</volume><issue>5</issue><elocation-id>e95403</elocation-id><history><date date-type="received"><day>29</day><month>1</month><year>2014</year></date><date date-type="accepted"><day>25</day><month>3</month><year>2014</year></date></history><permissions><copyright-year>2014</copyright-year><copyright-holder>Lazo et al</copyright-holder><license><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><abstract><sec><title>Aim</title><p>We aimed to estimate the morbidity rate and associated factors for diabetic peripheral neuropathy (DPN) in a low-middle income country setting.</p></sec><sec><title>Methods</title><p>Cross-sectional study, data was gathered at Peru's Ministry of Health national specialized hospital for endocrinological conditions through standardized interviews, anthropometric measurements and blood tests for glycated haemoglobin (HbA1c). DPN was evaluated using two techniques: the Semmes-Weinstein monofilament test and the diabetic neuropathy symptom score. Overall prevalence and 95% confidence intervals (95% CI) were calculated. Potential factors related to DPN explored included body mass index, years with disease (<10 vs. ≥10 years), glycaemic control (HbA1c <7% vs. ≥7%), microalbuminuria, retinopathy, and current pharmacological treatment. Multivariable analysis was performed using Poisson analysis to calculate prevalence ratios.</p></sec><sec><title>Results</title><p>DPN was observed in 73/129 (56.6%) patients. In multivariable analysis adjusted by age and sex, the prevalence ratio of neuropathy was 1.4 times higher (95% CI 1.07–1.88) in patients who took insulin plus metformin compared to patients who used one treatment alone, and 1.4 higher (95% CI 1.02–1.93) in patients with ≥10 years of disease compared to those with a shorter duration of disease. Also we found some characteristics in foot evaluation associated to neuropathy such as deformities (p<0.001), onychomycosis (p = 0.012), abnormal Achilles reflex (p<0.001), pain perception (p<0.001) and vibration perception (p<0.001).</p></sec><sec><title>Conclusion</title><p>DPN is highly frequent among patients with diabetes in a national specialized facility from Peru. Associated factors to DPN included being a diabetic patient for over ten years, and receiving insulin plus metformin</p></sec></abstract><funding-group><funding-statement>ML, ABO, KS, GM, JJM, RHG are affiliated with the CRONICAS Centre of Excellence in Chronic Diseases at Universidad Peruana Cayetano Heredia supported by the National Heart, Lung, and Blood Institute Global Health Initiative under the contract Global Health Activities in Developing Countries to Combat Non-Communicable Chronic Diseases (Project Number 268200900033C). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="5"></page-count></counts></article-meta></front><body><sec id="s1"><title>Introduction</title><p>Type-2 diabetes mellitus (T2DM) constitutes a major challenge in low-middle income countries (LMIC): only 3.6% of patients in Latin America achieve the three American Diabetes Association (ADA) recommended targets for blood pressure, LDL cholesterol, and HbA1C <xref rid="pone.0095403-Chan1" ref-type="bibr">[1]</xref>. This demonstrates that a significant gap between recommended diabetes care and the care patients actually receive exists in LMIC.</p><p>Diabetic foot neuropathy is one of the most important complications and can have a huge impact on patients, families, and society. Cross-sectional studies from LMIC found prevalence rates of DPN between 22%–60% <xref rid="pone.0095403-Tres1" ref-type="bibr">[2]</xref>, <xref rid="pone.0095403-Bos1" ref-type="bibr">[3]</xref>, and up to 25% of them will develop a foot ulcer <xref rid="pone.0095403-Singh1" ref-type="bibr">[4]</xref>. Eighty-five percent of lower-limb amputations are preceded by foot ulceration <xref rid="pone.0095403-Palumbo1" ref-type="bibr">[5]</xref>, and 5-year mortality following amputation is 44.3%<xref rid="pone.0095403-Tentolouris1" ref-type="bibr">[6]</xref>. Improvements in foot ulceration diagnosis and prevention can reduce amputation risk and reduce health care costs <xref rid="pone.0095403-Ollendorf1" ref-type="bibr">[7]</xref>. Prior to assessing appropriate methods to diagnose and prevent these complications, it is necessary to better understand the prevalence and characterize associated risk factors in our population. Therefore, the primary objective of the study was to determine the prevalence of DPN in ambulatory patients in a general national hospital in an LMIC setting and the secondary objective was to explore associated factors for DPN in this population.</p></sec><sec sec-type="methods" id="s2"><title>Methods</title><sec id="s2a"><title>Ethics Statement</title><p>Hospital Nacional Cayetano Heredia's (HNCH) Ethics Committee approved the study protocol and written informed consent was obtained from all participants.</p></sec><sec id="s2b"><title>Study Design and participants</title><p>We conducted a cross-sectional study between July and August 2012 at the diabetes outpatient clinic of HNCH in Lima, Peru. Recruitment strategy was convenience sampling strategy of patients receiving care in this facility, selected by Peru's Ministry of Health as the national specialized hospital for endocrinological conditions <xref rid="pone.0095403-Ministerio1" ref-type="bibr">[8]</xref>. Inclusion criteria were T2DM diagnosis according to ADA criteria (HbA1c ≥6.5% or Fasting plasma glucose ≥126 mg/dl or two-hour plasma glucose ≥200 mg/dl during an oral glucose tolerance test or a random plasma glucose ≥200 mg/dl) and age ≥18 years old. Patients with gestational diabetes mellitus and secondary diabetes (steroid-induced, cystic fibrosis, hemochromatosis and chronic pancreatitis) were excluded <xref rid="pone.0095403-American1" ref-type="bibr">[9]</xref>.</p></sec><sec id="s2c"><title>Assessments and outcome measures</title><p>Venous blood samples were evaluated for glycated haemoglobin (HbA1c) using high-performance liquid chromatography (D10-BIORAD, Germany). According to ADA guidelines, glycaemic control was defined as HbA1c <7.0% and blood pressure control as <140/80 mmHg <xref rid="pone.0095403-American2" ref-type="bibr">[10]</xref>.</p><p>Potential factors related to DPN explored included body mass index, years with disease (<10/≥10 years), glycaemic control (HbA1c <7%/≥7%), microalbuminuria, retinopathy, and current pharmacological treatment. Drug treatment was categorized into oral hypoglycaemic agents (OHA), insulin, and OHA plus insulin. Urine samples were assessed for microalbuminuria using commercial test strips following manufacturer's instructions: albumin concentrations ≥20 mg/L are consistent with microalbuminuria (albumin >30 mg/day). Retinopathy was evaluated through a fundoscopy exam by an ophthalmologist.</p><p>We completed a checklist to assess characteristics of the appearance of the feet, noting deformities, dry skin, calluses, muscle wasting (guttering between metatarsals), onychogryphosis (hypertrophic nails), onychomycosis, infection, and cracks. We also performed vascular and neurological evaluations. For the vascular evaluation, palpation of the dorsalis pedis pulse was performed using fingertips and the presence or absence was recorded. Sensory neurological evaluation consisted of: (i) ankle jerk (Achilles reflex), (ii) pain perception using a sterile pin in the dorsum of the great toe, and (iii) vibration with a 128-Hz tuning fork.</p><p>Additionally, we performed the Semmes-Weinstein monofilament (SWF) test and the 4-item diabetic neuropathy symptom (DNS) score. Nylon monofilaments were constructed to buckle when a 10-g force was applied, and loss of the ability to detect this pressure on the plantar surface of the foot indicated loss of large-fibre nerve function. Two sites of the foot, first metatarsal heads and plantar area of the heel were examined <xref rid="pone.0095403-Boulton1" ref-type="bibr">[11]</xref>. Inability to feel a SWF was considered to be indicative of high risk for foot ulceration <xref rid="pone.0095403-McNeely1" ref-type="bibr">[12]</xref>. The DNS score was validated by Meijer <italic>et al</italic>. <xref rid="pone.0095403-Meijer1" ref-type="bibr">[13]</xref> and consists of the following self-reported items: (1) unsteadiness during walking, (2) pain, burning or aching of the legs or feet, (3) prickling sensations in the legs or feet, and (4) numbness in the legs or feet. Presence is scored as 1 point, absence as 0 points, with a maximum score of 4 points. A DNS score of ≥1 point is considered positive. The same physician performed all of the SWF and DNS tests in the same patient. DPN was defined as a negative SWF test at one point and/or a DNS score between 1 and 4.</p></sec><sec id="s2d"><title>Statistical methods</title><p>The calculated sample size was 114, which assumed a 40% prevalence of neuropathy, <xref rid="pone.0095403-MenchacaDaz1" ref-type="bibr">[14]</xref> 0.09 precision and 0.05 significance. Prevalence and 95% confidence intervals (95% CI) were calculated. Chi-square or Fisher's exact test, where appropriate, were used to explore potential factors related to DPN. Multivariable analysis was performed using Poisson analysis for calculating prevalence ratios. STATA 11 for Windows (Stata Corp, College Station, TX) was used for analysis.</p></sec></sec><sec id="s3"><title>Results</title><p>A total of 129 T2DM patients, 73 (56.6%) females, mean age 59.2 years (SD ±8.6), were enrolled in the study. Mean body mass index was 28.9 Kg/m<sup>2</sup> (SD ±5.2), mean duration of T2DM was 8.6 years (SD ±6.5) and mean HbA1c was 8.7% (SD ±2.2). Mean systolic and diastolic blood pressure were 121.5 mm Hg (SD ±22.3) and 70.9 mm Hg (SD ±11.0), respectively. Sixty-two patients (48.0%) took OHA as treatment for their diabetes, while 12 (9.3%) took insulin alone, and 28 (21.7%) took OHA + insulin.</p><p>DPN was present in 73 (56.6%; 95% CI 47.9%–65.2%) patients. Of these, 49 (37.9%) patients had a positive DNS score and 51 (39.5%) patients had a negative response to SWF; 27 (20.9%) patients were positive on both tests.</p><p>Only 26.4% (95% CI 18.6%–34.1%) of the study population met the ADA glycaemic goal, while 71.3% (95% CI 62.7%–78.9%) met the ADA blood pressure goal. Forty-two (32.5%; 95% CI 24.3%–40.7%) patients took anti hypertensive drugs. Characteristics of the population with and without neuropathy are presented in <xref ref-type="table" rid="pone-0095403-t001">Table 1</xref>. <xref ref-type="table" rid="pone-0095403-t002">Table 2</xref> shows the results of the evaluation of the appearance of the feet, the vascular evaluation, and the neurological assessment with respect to DPN.</p><table-wrap id="pone-0095403-t001" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0095403.t001</object-id><label>Table 1</label><caption><title>Characteristics of the study population according to neuropathy.</title></caption><alternatives><graphic id="pone-0095403-t001-1" xlink:href="pone.0095403.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></colgroup><thead><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Neuropathy (N = 73)</td><td align="left" rowspan="1" colspan="1">Without neuropathy (N = 56)</td><td align="left" rowspan="1" colspan="1">p-value</td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Sex</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"><bold> Female</bold></td><td align="left" rowspan="1" colspan="1">42 (57.5%)</td><td align="left" rowspan="1" colspan="1">31 (42.5%)</td><td align="left" rowspan="1" colspan="1">0.80</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Male</bold></td><td align="left" rowspan="1" colspan="1">31 (55.3%)</td><td align="left" rowspan="1" colspan="1">25 (44. 6%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Age</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"><bold> <60 years</bold></td><td align="left" rowspan="1" colspan="1">33 (50.7%)</td><td align="left" rowspan="1" colspan="1">32 (49.2%)</td><td align="left" rowspan="1" colspan="1">0.17</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥60 years</bold></td><td align="left" rowspan="1" colspan="1">40 (62.5%)</td><td align="left" rowspan="1" colspan="1">24 (37.5%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Body Mass Index</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"><bold> <25</bold></td><td align="left" rowspan="1" colspan="1">12 (57.1%)</td><td align="left" rowspan="1" colspan="1">9 (42.9%)</td><td align="left" rowspan="1" colspan="1">0.66</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥25 and <30</bold></td><td align="left" rowspan="1" colspan="1">31 (52.5%)</td><td align="left" rowspan="1" colspan="1">28(47.5%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥30</bold></td><td align="left" rowspan="1" colspan="1">30 (61.2%)</td><td align="left" rowspan="1" colspan="1">19 (38.85%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Years with disease</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"><bold> <10 years</bold></td><td align="left" rowspan="1" colspan="1">31 (45.6%)</td><td align="left" rowspan="1" colspan="1">37 (54.4%)</td><td align="left" rowspan="1" colspan="1">0.008</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥10 years</bold></td><td align="left" rowspan="1" colspan="1">42 (68.8%)</td><td align="left" rowspan="1" colspan="1">19 (31.2%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Glycated haemoglobin</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"><bold> <7%</bold></td><td align="left" rowspan="1" colspan="1">17 (50%)</td><td align="left" rowspan="1" colspan="1">17 (50%)</td><td align="left" rowspan="1" colspan="1">0.36</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥7%</bold></td><td align="left" rowspan="1" colspan="1">56 (58.6%)</td><td align="left" rowspan="1" colspan="1">39 (41.1%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">MIcroalbuminuria</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"><bold> Negative</bold></td><td align="left" rowspan="1" colspan="1">57 (56.4%)</td><td align="left" rowspan="1" colspan="1">44 (43.5%)</td><td align="left" rowspan="1" colspan="1">0.94</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Positive</bold></td><td align="left" rowspan="1" colspan="1">16 (57.1%)</td><td align="left" rowspan="1" colspan="1">12 (42.8%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Retinopathy</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"><bold> Yes</bold></td><td align="left" rowspan="1" colspan="1">19 (73.1%)</td><td align="left" rowspan="1" colspan="1">7 (26.9%)</td><td align="left" rowspan="1" colspan="1">0.048</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> No</bold></td><td align="left" rowspan="1" colspan="1">52 (51.4%)</td><td align="left" rowspan="1" colspan="1">49 (48.5%)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Treatment</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"><bold> Any other treatment</bold></td><td align="left" rowspan="1" colspan="1">51 (50.5%)</td><td align="left" rowspan="1" colspan="1">50 (49.5%)</td><td align="left" rowspan="1" colspan="1">0.008</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> OHA</bold><xref ref-type="table-fn" rid="nt102">**</xref><bold>+ insulin</bold></td><td align="left" rowspan="1" colspan="1">22 (78.6%)</td><td align="left" rowspan="1" colspan="1">6 (21.4%)</td><td align="left" rowspan="1" colspan="1"></td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt101"><label></label><p>*Percentages were calculated by rows.</p></fn><fn id="nt102"><label></label><p>**OHA: Oral hypoglycaemic agent.</p></fn></table-wrap-foot></table-wrap><table-wrap id="pone-0095403-t002" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0095403.t002</object-id><label>Table 2</label><caption><title>Characteristics of foot evaluation.</title></caption><alternatives><graphic id="pone-0095403-t002-2" xlink:href="pone.0095403.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></colgroup><thead><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Neuropathy (N = 73)</td><td align="left" rowspan="1" colspan="1">Without neuropathy (N = 56)</td><td align="left" rowspan="1" colspan="1"></td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Appearance of feet</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"><bold> Deformities</bold></td><td align="left" rowspan="1" colspan="1">27(37.0%)</td><td align="left" rowspan="1" colspan="1">4 (7.14%)</td><td align="left" rowspan="1" colspan="1"><0.001<xref ref-type="table-fn" rid="nt103">*</xref></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Drew skin, calluses</bold></td><td align="left" rowspan="1" colspan="1">68(93.2%)</td><td align="left" rowspan="1" colspan="1">52 (92.8%)</td><td align="left" rowspan="1" colspan="1">0.948</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Hypotrophy interosseous</bold></td><td align="left" rowspan="1" colspan="1">38(52.1%)</td><td align="left" rowspan="1" colspan="1">19 (33.9%)</td><td align="left" rowspan="1" colspan="1">0.05</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Onychogryphosis</bold></td><td align="left" rowspan="1" colspan="1">26(35.6%)</td><td align="left" rowspan="1" colspan="1">13 (23.2%)</td><td align="left" rowspan="1" colspan="1">0.12</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Onychomycosis</bold></td><td align="left" rowspan="1" colspan="1">62 (84.9%)</td><td align="left" rowspan="1" colspan="1">36 (54.2%)</td><td align="left" rowspan="1" colspan="1">0.012<xref ref-type="table-fn" rid="nt103">*</xref></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Infection</bold></td><td align="left" rowspan="1" colspan="1">1 (1.37%)</td><td align="left" rowspan="1" colspan="1">-</td><td align="left" rowspan="1" colspan="1">0.37</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Cracks</bold></td><td align="left" rowspan="1" colspan="1">25 (34.2%)</td><td align="left" rowspan="1" colspan="1">13 (22.1%)</td><td align="left" rowspan="1" colspan="1">0.17</td></tr><tr><td align="left" rowspan="1" colspan="1">Vascular evaluation</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"><bold> Dorsalis pedis pulse absent</bold></td><td align="left" rowspan="1" colspan="1">2 (2.7%)</td><td align="left" rowspan="1" colspan="1">2 (3.6%)</td><td align="left" rowspan="1" colspan="1">0.78</td></tr><tr><td align="left" rowspan="1" colspan="1">Neurological evaluation</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"><bold>Achilles Reflex abnormal</bold></td><td align="left" rowspan="1" colspan="1">63 (86.3%)</td><td align="left" rowspan="1" colspan="1">20 (35.7%)</td><td align="left" rowspan="1" colspan="1"><0.001<xref ref-type="table-fn" rid="nt103">*</xref></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Pain perception abnormal</bold></td><td align="left" rowspan="1" colspan="1">46 (63.1%)</td><td align="left" rowspan="1" colspan="1">6 (10.7%)</td><td align="left" rowspan="1" colspan="1"><0.001<xref ref-type="table-fn" rid="nt103">*</xref></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Vibration perception abnormal</bold></td><td align="left" rowspan="1" colspan="1">32 (43.8%)</td><td align="left" rowspan="1" colspan="1">7 (12.5%)</td><td align="left" rowspan="1" colspan="1"><0.001<xref ref-type="table-fn" rid="nt103">*</xref></td></tr><tr><td align="left" rowspan="1" colspan="1">Ulceration</td><td align="left" rowspan="1" colspan="1">1 (1.37%)</td><td align="left" rowspan="1" colspan="1">1 (1.79%)</td><td align="left" rowspan="1" colspan="1"></td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt103"><label></label><p>*Fisher exact test.</p></fn></table-wrap-foot></table-wrap><p>In the multivariable model, years of disease and treatment with OHA plus insulin were factors associated with increased prevalence of DPN (<xref ref-type="table" rid="pone-0095403-t003">Table 3</xref>).</p><table-wrap id="pone-0095403-t003" orientation="portrait" position="float"><object-id pub-id-type="doi">10.1371/journal.pone.0095403.t003</object-id><label>Table 3</label><caption><title>Factors associated with Diabetic Peripheral Neuropathy.</title></caption><alternatives><graphic id="pone-0095403-t003-3" xlink:href="pone.0095403.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></colgroup><thead><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Bivariable model Prevalence ratio (95% CI)</td><td align="left" rowspan="1" colspan="1">Multivariable model<xref ref-type="table-fn" rid="nt104">*</xref> Prevalence ratio (95% CI)</td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Sex</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"><bold> Female</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Male</bold></td><td align="left" rowspan="1" colspan="1">0.96 (0.71–1.31)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Age</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"><bold> <60 years</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥60 years</bold></td><td align="left" rowspan="1" colspan="1">1.23 (0.91–1.67)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Body Mass Index</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"><bold> <25</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥25 and <30</bold></td><td align="left" rowspan="1" colspan="1">0.92 (0.59–1.43)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥30</bold></td><td align="left" rowspan="1" colspan="1">1.07 (0.69–1.65)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Years with disease</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"><bold> <10 years</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1">1 (Reference)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥10 years</bold></td><td align="left" rowspan="1" colspan="1">1.51 (1.11–2.06)</td><td align="left" rowspan="1" colspan="1">1.41 (1.03–1.93)</td></tr><tr><td align="left" rowspan="1" colspan="1">Glycated haemoglobin</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"><bold> <7%</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> ≥7%</bold></td><td align="left" rowspan="1" colspan="1">1.18 (0.81–1.72)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">MIcroalbuminuria</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"><bold> Negative</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Positive</bold></td><td align="left" rowspan="1" colspan="1">1.01 (0.70–1.46)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Retinopathy</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"><bold> No</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Yes</bold></td><td align="left" rowspan="1" colspan="1">1.42 (1.05–1.92)</td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Treatment</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"><bold> Any other treatment</bold></td><td align="left" rowspan="1" colspan="1">1 (Reference)</td><td align="left" rowspan="1" colspan="1">1 (Reference)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold> Metformin + insulin</bold></td><td align="left" rowspan="1" colspan="1">1.56 (1.18–2.05)</td><td align="left" rowspan="1" colspan="1">1.43 (1.08–1.89)</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="nt104"><label></label><p>*Variables independently associated with DPN.</p></fn></table-wrap-foot></table-wrap></sec><sec id="s4"><title>Discussion</title><p>We found that DPN is highly frequent among patients with T2DM in a national specialized facility from Peru. According to the literature, DPN prevalence varies from 10% to 75% <xref rid="pone.0095403-Karvestedt1" ref-type="bibr">[15]</xref>–<xref rid="pone.0095403-Janghorbani1" ref-type="bibr">[17]</xref>, a wide range that reflects differences among countries, settings, diagnostic methods, population characteristics, and quality of care. Only two studies have presented data on DPN prevalence in Latin American countries. One study in an outpatient clinic in Brazil found a prevalence of 22%–46% depending on method used—nerve conduction and the Michigan questionnaire, respectively <xref rid="pone.0095403-Tres1" ref-type="bibr">[2]</xref>. Another study in Mexico found a prevalence of 69% when evaluating DPN by the Michigan questionnaire <xref rid="pone.0095403-Ibarra1" ref-type="bibr">[18]</xref>. The lack of data on DPN in Latin American countries underscores the need for further investigations of its epidemiology.</p><p>In our study, more than half of the T2DM patients had peripheral neuropathy when evaluated by the DNS score and SWF test, both techniques have high sensitivity, a characteristic that is ideal for screening. However, we did not use the gold standard of nerve conduction, and thus we may have overestimated the prevalence of DPN within this sample. Nerve conduction is too expensive for regular use in LMIC, and it is important to investigate alternative cheaper diagnostic approaches. However, future studies should perform more extensive comparisons of DPN in Latin American countries using a standard method.</p><p>Most previous studies found that duration of diabetes, insulin treatment, proteinuria, and presence of retinopathy are factors associated with DPN <xref rid="pone.0095403-Kiani1" ref-type="bibr">[19]</xref>, <xref rid="pone.0095403-Mold1" ref-type="bibr">[20]</xref>, and our results are consistent with these findings. Drug treatment is an important risk factor for neuropathy, which may be related to the duration of disease. In one cohort study, patients receiving insulin monotherapy and insulin plus metformin were twice as likely to develop neuropathy when compared to patients taking metformin alone <xref rid="pone.0095403-Currie1" ref-type="bibr">[21]</xref>. Similarly, we found that patients taking insulin plus OHA were 40% more likely to have DPN, as were those with more than 10 years of disease. This finding clearly shows that patients with severe disease, that need more than one treatment scheme are most likely to have neuropathy.</p><p>Our work in Peru reveals a very low prevalence of glycaemic control among patients with T2DM. Previous studies demonstrate that foot deformities and other ulcer risk factors are exacerbated by poor glucose control and longer duration of diabetes <xref rid="pone.0095403-Chung1" ref-type="bibr">[22]</xref>. Similarly, the prevalence of complications such as foot ulcers is significantly higher in patients with higher HbA1c levels <xref rid="pone.0095403-Chuang1" ref-type="bibr">[23]</xref>. Together with the associated chronic complications, this constitutes a major health concern in LMIC such as Peru.</p><p>A major limitation of our study is the selection of patients with T2DM from a single facility. However, according to Peru's Ministry of Health, this study site has the status of leading national specialized hospital for endocrinological conditions <xref rid="pone.0095403-Ministerio1" ref-type="bibr">[8]</xref>. Thus, characterizing DPN in this hospital is of enormous importance for establishing bench marks in the care patients with diabetes in Peru as well as to guide future policy and quality improvement developments.</p><p>Based on our findings, we can expect to find high rates of long-term diabetes-related complications in Peru if control strategies are not implemented. While our results are not necessarily directly translatable to other centres, they emphasize the need for developing monitoring and evaluation approaches that are appropriate in resource-constrained settings. Screening of high-risk individuals, early detection, and proper management of DPN in patients with T2DM should be mandatory. As per guidelines, careful foot examination at each visit to the outpatient clinic, active application of screening tools every year, and an organized diabetic foot care program should be implemented to prevent complications in patients with T2DM</p></sec></body><back><ack><p>Yvonne Huaylinos, Talia Stewart and Alana Lerner for their support in data collection.</p></ack><ref-list><title>References</title><ref id="pone.0095403-Chan1"><label>1</label><mixed-citation publication-type="journal"><name><surname>Chan</surname><given-names>JC</given-names></name>, <name><surname>Gagliardino</surname><given-names>JJ</given-names></name>, <name><surname>Baik</surname><given-names>SH</given-names></name>, <name><surname>Chantelot</surname><given-names>JM</given-names></name>, <name><surname>Ferreira</surname><given-names>SR</given-names></name>, <etal>et al</etal> (<year>2009</year>) <article-title>Multifaceted determinants for achieving glycemic control: the International Diabetes Management Practice Study (IDMPS)</article-title>. <source>Diabetes Care</source><volume>32</volume>: <fpage>227</fpage>–<lpage>233</lpage><pub-id pub-id-type="pmid">19033410</pub-id></mixed-citation></ref><ref id="pone.0095403-Tres1"><label>2</label><mixed-citation publication-type="journal"><name><surname>Tres</surname><given-names>GS</given-names></name>, <name><surname>Lisbôa</surname><given-names>HR</given-names></name>, <name><surname>Syllos</surname><given-names>R</given-names></name>, <name><surname>Canani</surname><given-names>LH</given-names></name>, <name><surname>Gross</surname><given-names>JL</given-names></name> (<year>2007</year>) <article-title>Prevalence and characteristics of diabetic polyneuropathy in Passo Fundo, South of Brazil</article-title>. <source>Arq Bras Endocrinol Metabol</source><volume>51</volume>: <fpage>987</fpage>–<lpage>992</lpage><pub-id pub-id-type="pmid">17934667</pub-id></mixed-citation></ref><ref id="pone.0095403-Bos1"><label>3</label><mixed-citation publication-type="journal"><name><surname>Bos</surname><given-names>M</given-names></name>, <name><surname>Agyemang</surname><given-names>C</given-names></name> (<year>2013</year>) <article-title>Prevalence and complications of diabetes mellitus in Northern Africa, a systematic review</article-title>. <source>BMC Public Health</source><volume>13</volume>: <fpage>387</fpage>–<lpage>393</lpage><pub-id pub-id-type="pmid">23617762</pub-id></mixed-citation></ref><ref id="pone.0095403-Singh1"><label>4</label><mixed-citation publication-type="journal"><name><surname>Singh</surname><given-names>N</given-names></name>, <name><surname>Armstrong</surname><given-names>DG</given-names></name>, <name><surname>Lipsky</surname><given-names>BA</given-names></name> (<year>2005</year>) <article-title>Preventing foot ulcers in patients with diabetes</article-title>. <source>JAMA</source><volume>293</volume>: <fpage>217</fpage>–<lpage>228</lpage><pub-id pub-id-type="pmid">15644549</pub-id></mixed-citation></ref><ref id="pone.0095403-Palumbo1"><label>5</label><mixed-citation publication-type="other">Palumbo PJ, Melton LJ 3rd. (1985) Peripheral vascular disease and diabetes. In: Diabetes in America: diabetes data compiled 1984. Washington, D.C.: Government Printing Office.</mixed-citation></ref><ref id="pone.0095403-Tentolouris1"><label>6</label><mixed-citation publication-type="journal"><name><surname>Tentolouris</surname><given-names>N</given-names></name>, <name><surname>Al-Sabbagh</surname><given-names>S</given-names></name>, <name><surname>Walker</surname><given-names>MG</given-names></name>, <name><surname>Boulton</surname><given-names>AJ</given-names></name>, <name><surname>Jude</surname><given-names>EB</given-names></name> (<year>2004</year>) <article-title>Mortality in diabetic and nondiabetic patients after amputations performed from 1990 to 1995: a 5-year follow-up study</article-title>. <source>Diabetes Care</source><volume>27</volume>: <fpage>1598</fpage>–<lpage>1604</lpage><pub-id pub-id-type="pmid">15220234</pub-id></mixed-citation></ref><ref id="pone.0095403-Ollendorf1"><label>7</label><mixed-citation publication-type="journal"><name><surname>Ollendorf</surname><given-names>DA</given-names></name>, <name><surname>Kotsanos</surname><given-names>JG</given-names></name>, <name><surname>Wishner</surname><given-names>WJ</given-names></name>, <name><surname>Friedman</surname><given-names>M</given-names></name>, <name><surname>Cooper</surname><given-names>T</given-names></name>, <name><surname>Bittoni</surname><given-names>M</given-names></name>, <name><surname>Oster</surname><given-names>G</given-names></name> (<year>1998</year>) <article-title>Potential economic benefits of lower-extremity amputation prevention strategies in diabetes</article-title>. <source>Diabetes Care</source><volume>21</volume>: <fpage>1240</fpage>–<lpage>1245</lpage><pub-id pub-id-type="pmid">9702427</pub-id></mixed-citation></ref><ref id="pone.0095403-Ministerio1"><label>8</label><mixed-citation publication-type="journal">Ministerio de Salud del Perú. Resolución Ministerial <volume>No 544</volume> . 02 July 2007.</mixed-citation></ref><ref id="pone.0095403-American1"><label>9</label><mixed-citation publication-type="journal"><collab>American Diabetes Association</collab> (<year>2010</year>) <article-title>Diagnosis and classification of diabetes mellitus</article-title>. <source>Diabetes Care</source><volume>33</volume>: <fpage>S62</fpage>–<lpage>69</lpage><pub-id pub-id-type="pmid">20042775</pub-id></mixed-citation></ref><ref id="pone.0095403-American2"><label>10</label><mixed-citation publication-type="journal"><collab>American Diabetes Association</collab> (<year>2013</year>) <article-title>Standards of medical care in diabetes—2013</article-title>. <source>Diabetes Care</source><volume>36</volume>: <fpage>S11</fpage>–<lpage>66</lpage><pub-id pub-id-type="pmid">23264422</pub-id></mixed-citation></ref><ref id="pone.0095403-Boulton1"><label>11</label><mixed-citation publication-type="journal"><name><surname>Boulton</surname><given-names>AJ</given-names></name>, <name><surname>Armstrong</surname><given-names>DG</given-names></name>, <name><surname>Albert</surname><given-names>SF</given-names></name>, <name><surname>Frykberg</surname><given-names>RG</given-names></name>, <name><surname>Hellman</surname><given-names>R</given-names></name>, <etal>et al</etal> (<year>2008</year>) <article-title>Comprehensive foot examination and risk assessment: a report of the task force of the foot care interest group of the American Diabetes Association, with endorsement by the American Association of Clinical Endocrinologists</article-title>. <source>Diabetes Care</source><volume>31</volume>: <fpage>1679</fpage>–<lpage>1685</lpage><pub-id pub-id-type="pmid">18663232</pub-id></mixed-citation></ref><ref id="pone.0095403-McNeely1"><label>12</label><mixed-citation publication-type="journal"><name><surname>McNeely</surname><given-names>MJ</given-names></name>, <name><surname>Boyko</surname><given-names>E</given-names></name>, <name><surname>Ahroni</surname><given-names>JH</given-names></name> (<year>1995</year>) <article-title>The independent contributions of diabetic neuropathy and vasculopathy in foot ulceration: how great are the risks?</article-title><source>Diabetes Care</source><volume>18</volume>: <fpage>216</fpage>–<lpage>219</lpage><pub-id pub-id-type="pmid">7729300</pub-id></mixed-citation></ref><ref id="pone.0095403-Meijer1"><label>13</label><mixed-citation publication-type="journal"><name><surname>Meijer</surname><given-names>JW</given-names></name>, <name><surname>Smit</surname><given-names>AJ</given-names></name>, <name><surname>Sonderen</surname><given-names>EV</given-names></name>, <name><surname>Groothoff</surname><given-names>JW</given-names></name>, <name><surname>Eisma</surname><given-names>WH</given-names></name>, <etal>et al</etal> (<year>2002</year>) <article-title>Symptom scoring systems to diagnose distal polyneuropathy in diabetes: the Diabetic Neuropathy Symptom score</article-title>. <source>Diabet Med</source><volume>19</volume>: <fpage>962</fpage>–<lpage>965</lpage><pub-id pub-id-type="pmid">12421436</pub-id></mixed-citation></ref><ref id="pone.0095403-MenchacaDaz1"><label>14</label><mixed-citation publication-type="journal"><name><surname>Menchaca-Díaz</surname><given-names>R</given-names></name>, <name><surname>Bogarín-López</surname><given-names>B</given-names></name>, <name><surname>Zamudio-Gómez</surname><given-names>MA</given-names></name>, <name><surname>Anzaldo-Campos</surname><given-names>MC</given-names></name> (<year>2012</year>) <article-title>[Severe periodontitis, edentulism and neuropathy in patients with type 2 diabetes mellitus]</article-title>. <source>Gac Med Mex</source><volume>148</volume>: <fpage>34</fpage>–<lpage>41</lpage><pub-id pub-id-type="pmid">22367307</pub-id></mixed-citation></ref><ref id="pone.0095403-Karvestedt1"><label>15</label><mixed-citation publication-type="journal"><name><surname>Karvestedt</surname><given-names>L</given-names></name>, <name><surname>Martensson</surname><given-names>E</given-names></name>, <name><surname>Grill</surname><given-names>V</given-names></name>, <name><surname>Elofsson</surname><given-names>S</given-names></name>, <name><surname>von Wendt</surname><given-names>G</given-names></name>, <etal>et al</etal> (<year>2011</year>) <article-title>The prevalence of peripheral neuropathy in a population-based study of patients with type 2 diabetes in Sweden</article-title>. <source>J Diabetes Complications</source><volume>25</volume>: <fpage>97</fpage>–<lpage>106</lpage><pub-id pub-id-type="pmid">20488731</pub-id></mixed-citation></ref><ref id="pone.0095403-Ko1"><label>16</label><mixed-citation publication-type="journal"><name><surname>Ko</surname><given-names>SH</given-names></name>, <name><surname>Cha</surname><given-names>BY</given-names></name> (<year>2012</year>) <article-title>Diabetic Peripheral Neuropathy in Type 2 Diabetes Mellitus in Korea</article-title>. <source>Diabetes Metab J</source><volume>36</volume>: <fpage>6</fpage>–<lpage>12</lpage><pub-id pub-id-type="pmid">22363916</pub-id></mixed-citation></ref><ref id="pone.0095403-Janghorbani1"><label>17</label><mixed-citation publication-type="journal"><name><surname>Janghorbani</surname><given-names>M</given-names></name>, <name><surname>Rezvanian</surname><given-names>H</given-names></name>, <name><surname>Kachooei</surname><given-names>A</given-names></name>, <name><surname>Ghorbani</surname><given-names>A</given-names></name>, <name><surname>Chitsaz</surname><given-names>A</given-names></name>, <etal>et al</etal> (<year>2006</year>) <article-title>Peripheral neuropathy in type 2 diabetes mellitus in Isfahan, Iran: prevalence and risk factors</article-title>. <source>Acta Neurol Scand</source><volume>114</volume>: <fpage>384</fpage>–<lpage>391</lpage><pub-id pub-id-type="pmid">17083338</pub-id></mixed-citation></ref><ref id="pone.0095403-Ibarra1"><label>18</label><mixed-citation publication-type="journal"><name><surname>Ibarra</surname><given-names>CT</given-names></name>, <name><surname>Rocha Jde</surname><given-names>J</given-names></name>, <name><surname>Hernández</surname><given-names>RO</given-names></name>, <name><surname>Nieves</surname><given-names>RE</given-names></name>, <name><surname>Leyva</surname><given-names>RJ</given-names></name> (<year>2012</year>) <article-title>[Prevalence of peripheral neuropathy among primary care type 2 diabetic patients]</article-title>. <source>Rev Med Chil</source><volume>140</volume>: <fpage>1126</fpage>–<lpage>1131</lpage><pub-id pub-id-type="pmid">23354633</pub-id></mixed-citation></ref><ref id="pone.0095403-Kiani1"><label>19</label><mixed-citation publication-type="journal">Kiani J, Moghimbeigi A, Azizkhani H, Kosarifard S. (2013) The prevalence and associated risk factors of peripheral diabetic neuropathy in Hamedan, Iran. Arch Iran Med <volume>16</volume>: :17–19.</mixed-citation></ref><ref id="pone.0095403-Mold1"><label>20</label><mixed-citation publication-type="journal"><name><surname>Mold</surname><given-names>JW</given-names></name>, <name><surname>Vesely</surname><given-names>SK</given-names></name>, <name><surname>Keyl</surname><given-names>BA</given-names></name>, <name><surname>Schenk</surname><given-names>JB</given-names></name>, <name><surname>Roberts</surname><given-names>M</given-names></name> (<year>2004</year>) <article-title>The prevalence, predictors, and consequences of peripheral sensory neuropathy in older patients</article-title>. <source>J Am Board Fam Pract</source><volume>17</volume>: <fpage>309</fpage>–<lpage>318</lpage><pub-id pub-id-type="pmid">15355943</pub-id></mixed-citation></ref><ref id="pone.0095403-Currie1"><label>21</label><mixed-citation publication-type="journal"><name><surname>Currie</surname><given-names>CJ</given-names></name>, <name><surname>Poole</surname><given-names>CD</given-names></name>, <name><surname>Evans</surname><given-names>M</given-names></name>, <name><surname>Peters</surname><given-names>JR</given-names></name>, <name><surname>Morgan</surname><given-names>CL</given-names></name> (<year>2013</year>) <article-title>Mortality and other important diabetes-related outcomes with insulin vs other antihyperglycemic therapies in type 2 diabetes</article-title>. <source>J Clin Endocrinol Metab</source><volume>98</volume>: <fpage>668</fpage>–<lpage>677</lpage><pub-id pub-id-type="pmid">23372169</pub-id></mixed-citation></ref><ref id="pone.0095403-Chung1"><label>22</label><mixed-citation publication-type="journal"><name><surname>Chung</surname><given-names>JO</given-names></name>, <name><surname>Cho</surname><given-names>DH</given-names></name>, <name><surname>Chung</surname><given-names>DJ</given-names></name>, <name><surname>Chung</surname><given-names>MY</given-names></name> (<year>2011</year>) <article-title>Association between diabetic polyneuropathy and cardiovascular complications in type 2 diabetic patients</article-title>. <source>Diabetes Metab J</source><volume>35</volume>: <fpage>390</fpage>–<lpage>396</lpage><pub-id pub-id-type="pmid">21977459</pub-id></mixed-citation></ref><ref id="pone.0095403-Chuang1"><label>23</label><mixed-citation publication-type="journal"><collab>Chuang LM, Tsai ST, Huang BY, Tai TY, Diabcare-Asia 1998 Study Group</collab> (<year>2002</year>) <article-title>The status of diabetes control in Asia—a cross- sectional survey of 24 317 patients with diabetes mellitus in 1998</article-title>. <source>Diabet Med</source><volume>19</volume>: <fpage>978</fpage>–<lpage>85</lpage><pub-id pub-id-type="pmid">12647837</pub-id></mixed-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
EXPLOR_STEP=$WICRI_ROOT/Wicri/Santé/explor/EdenteV1/Data/Pmc/Corpus
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000751 | SxmlIndent | more
Ou
HfdSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd -nk 000751 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien
|wiki= Wicri/Santé
|area= EdenteV1
|flux= Pmc
|étape= Corpus
|type= RBID
|clé= PMC:4006783
|texte= Diabetic Peripheral Neuropathy in Ambulatory Patients with Type 2 Diabetes in a General Hospital in a Middle Income Country: A Cross-Sectional Study
}}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/RBID.i -Sk "pubmed:24789071" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd \
| NlmPubMed2Wicri -a EdenteV1
| This area was generated with Dilib version V0.6.33. |  |