Non-Traditional Risk Factors of Albuminuria in the Pediatric Population: A Scoping Review
Identifieur interne : 002E65 ( Pmc/Corpus ); précédent : 002E64; suivant : 002E66Non-Traditional Risk Factors of Albuminuria in the Pediatric Population: A Scoping Review
Auteurs : Erick Sierra-Diaz ; Alfredo De Jesus Celis-De La Rosa ; Felipe Lozano-Kasten ; Alejandro Bravo-Cuellar ; Mariana Garcia-Gutierrez ; Hernandez-Flores GeorginaSource :
- International Journal of Environmental Research and Public Health [ 1661-7827 ] ; 2017.
Abstract
The presence of albumin in urine has been used for more than four decades as a marker of renal and cardiovascular damage. Most of the information on this marker is related to adults. The prevalence of albuminuria in the pediatric population has been reported as being 2.2–12.8% in some countries. Most research in this field is related to albuminuria and diseases, such as diabetes and hypertension. Using the methodology described by Arksey and O’Malley in 2005, a scoping review was carried out to show that the presence of albumin in urine in the pediatric population might be associated with environmental, demographic, congenital, infectious, and non-infectious factors. The information collected is supported by 74 references present in PubMed. The results reveal the multiple causes associated with albuminuria in the pediatric population. This information can be very useful for clinical practice by adding knowledge about albuminuria behavior in children.
Url:
DOI: 10.3390/ijerph14101231
PubMed: 29035316
PubMed Central: 5664732
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PMC:5664732Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Non-Traditional Risk Factors of Albuminuria in the Pediatric Population: A Scoping Review</title><author><name sortKey="Sierra Diaz, Erick" sort="Sierra Diaz, Erick" uniqKey="Sierra Diaz E" first="Erick" last="Sierra-Diaz">Erick Sierra-Diaz</name><affiliation><nlm:aff id="af1-ijerph-14-01231">Public Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>alfredo_celis@yahoo.com</email></nlm:aff></affiliation></author><author><name sortKey="Celis De La Rosa, Alfredo De Jesus" sort="Celis De La Rosa, Alfredo De Jesus" uniqKey="Celis De La Rosa A" first="Alfredo De Jesus" last="Celis-De La Rosa">Alfredo De Jesus Celis-De La Rosa</name><affiliation><nlm:aff id="af1-ijerph-14-01231">Public Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>alfredo_celis@yahoo.com</email></nlm:aff></affiliation></author><author><name sortKey="Lozano Kasten, Felipe" sort="Lozano Kasten, Felipe" uniqKey="Lozano Kasten F" first="Felipe" last="Lozano-Kasten">Felipe Lozano-Kasten</name><affiliation><nlm:aff id="af2-ijerph-14-01231">Environmental Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>f_lozano_k@hotmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Bravo Cuellar, Alejandro" sort="Bravo Cuellar, Alejandro" uniqKey="Bravo Cuellar A" first="Alejandro" last="Bravo-Cuellar">Alejandro Bravo-Cuellar</name><affiliation><nlm:aff id="af3-ijerph-14-01231">Immunology Department, Western Research Biomedical Center (IMSS), Sierra Mojada 800, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>abravoc@prodigy.net.mx</email> (A.B.-C.);<email>gina.geodic1967@gmail.com</email> (H.-F.G.)</nlm:aff></affiliation></author><author><name sortKey="Garcia Gutierrez, Mariana" sort="Garcia Gutierrez, Mariana" uniqKey="Garcia Gutierrez M" first="Mariana" last="Garcia-Gutierrez">Mariana Garcia-Gutierrez</name><affiliation><nlm:aff id="af4-ijerph-14-01231">Pediatrics Department, Hospital Angeles del Carmen, Health Services, Tarascos 3473 Interior 240A, Fraccionamiento Monraz, Guadalajara, Jalisco 44670, Mexico;<email>mariana.endoc@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Georgina, Hernandez Flores" sort="Georgina, Hernandez Flores" uniqKey="Georgina H" first="Hernandez-Flores" last="Georgina">Hernandez-Flores Georgina</name><affiliation><nlm:aff id="af3-ijerph-14-01231">Immunology Department, Western Research Biomedical Center (IMSS), Sierra Mojada 800, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>abravoc@prodigy.net.mx</email> (A.B.-C.);<email>gina.geodic1967@gmail.com</email> (H.-F.G.)</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29035316</idno><idno type="pmc">5664732</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5664732</idno><idno type="RBID">PMC:5664732</idno><idno type="doi">10.3390/ijerph14101231</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">002E65</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002E65</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Non-Traditional Risk Factors of Albuminuria in the Pediatric Population: A Scoping Review</title><author><name sortKey="Sierra Diaz, Erick" sort="Sierra Diaz, Erick" uniqKey="Sierra Diaz E" first="Erick" last="Sierra-Diaz">Erick Sierra-Diaz</name><affiliation><nlm:aff id="af1-ijerph-14-01231">Public Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>alfredo_celis@yahoo.com</email></nlm:aff></affiliation></author><author><name sortKey="Celis De La Rosa, Alfredo De Jesus" sort="Celis De La Rosa, Alfredo De Jesus" uniqKey="Celis De La Rosa A" first="Alfredo De Jesus" last="Celis-De La Rosa">Alfredo De Jesus Celis-De La Rosa</name><affiliation><nlm:aff id="af1-ijerph-14-01231">Public Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>alfredo_celis@yahoo.com</email></nlm:aff></affiliation></author><author><name sortKey="Lozano Kasten, Felipe" sort="Lozano Kasten, Felipe" uniqKey="Lozano Kasten F" first="Felipe" last="Lozano-Kasten">Felipe Lozano-Kasten</name><affiliation><nlm:aff id="af2-ijerph-14-01231">Environmental Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>f_lozano_k@hotmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Bravo Cuellar, Alejandro" sort="Bravo Cuellar, Alejandro" uniqKey="Bravo Cuellar A" first="Alejandro" last="Bravo-Cuellar">Alejandro Bravo-Cuellar</name><affiliation><nlm:aff id="af3-ijerph-14-01231">Immunology Department, Western Research Biomedical Center (IMSS), Sierra Mojada 800, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>abravoc@prodigy.net.mx</email> (A.B.-C.);<email>gina.geodic1967@gmail.com</email> (H.-F.G.)</nlm:aff></affiliation></author><author><name sortKey="Garcia Gutierrez, Mariana" sort="Garcia Gutierrez, Mariana" uniqKey="Garcia Gutierrez M" first="Mariana" last="Garcia-Gutierrez">Mariana Garcia-Gutierrez</name><affiliation><nlm:aff id="af4-ijerph-14-01231">Pediatrics Department, Hospital Angeles del Carmen, Health Services, Tarascos 3473 Interior 240A, Fraccionamiento Monraz, Guadalajara, Jalisco 44670, Mexico;<email>mariana.endoc@gmail.com</email></nlm:aff></affiliation></author><author><name sortKey="Georgina, Hernandez Flores" sort="Georgina, Hernandez Flores" uniqKey="Georgina H" first="Hernandez-Flores" last="Georgina">Hernandez-Flores Georgina</name><affiliation><nlm:aff id="af3-ijerph-14-01231">Immunology Department, Western Research Biomedical Center (IMSS), Sierra Mojada 800, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>abravoc@prodigy.net.mx</email> (A.B.-C.);<email>gina.geodic1967@gmail.com</email> (H.-F.G.)</nlm:aff></affiliation></author></analytic><series><title level="j">International Journal of Environmental Research and Public Health</title><idno type="ISSN">1661-7827</idno><idno type="eISSN">1660-4601</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The presence of albumin in urine has been used for more than four decades as a marker of renal and cardiovascular damage. Most of the information on this marker is related to adults. The prevalence of albuminuria in the pediatric population has been reported as being 2.2–12.8% in some countries. Most research in this field is related to albuminuria and diseases, such as diabetes and hypertension. Using the methodology described by Arksey and O’Malley in 2005, a scoping review was carried out to show that the presence of albumin in urine in the pediatric population might be associated with environmental, demographic, congenital, infectious, and non-infectious factors. The information collected is supported by 74 references present in PubMed. The results reveal the multiple causes associated with albuminuria in the pediatric population. This information can be very useful for clinical practice by adding knowledge about albuminuria behavior in children.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Peterson, P A" uniqKey="Peterson P">P.A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Environ Res Public Health</journal-id><journal-id journal-id-type="iso-abbrev">Int J Environ Res Public Health</journal-id><journal-id journal-id-type="publisher-id">ijerph</journal-id><journal-title-group><journal-title>International Journal of Environmental Research and Public Health</journal-title></journal-title-group><issn pub-type="ppub">1661-7827</issn><issn pub-type="epub">1660-4601</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">29035316</article-id><article-id pub-id-type="pmc">5664732</article-id><article-id pub-id-type="doi">10.3390/ijerph14101231</article-id><article-id pub-id-type="publisher-id">ijerph-14-01231</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Non-Traditional Risk Factors of Albuminuria in the Pediatric Population: A Scoping Review</article-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-1006-9012</contrib-id><name><surname>Sierra-Diaz</surname><given-names>Erick</given-names></name><xref ref-type="aff" rid="af1-ijerph-14-01231">1</xref><xref rid="c1-ijerph-14-01231" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><name><surname>Celis-de la Rosa</surname><given-names>Alfredo de Jesus</given-names></name><xref ref-type="aff" rid="af1-ijerph-14-01231">1</xref></contrib><contrib contrib-type="author"><name><surname>Lozano-Kasten</surname><given-names>Felipe</given-names></name><xref ref-type="aff" rid="af2-ijerph-14-01231">2</xref></contrib><contrib contrib-type="author"><name><surname>Bravo-Cuellar</surname><given-names>Alejandro</given-names></name><xref ref-type="aff" rid="af3-ijerph-14-01231">3</xref></contrib><contrib contrib-type="author"><name><surname>Garcia-Gutierrez</surname><given-names>Mariana</given-names></name><xref ref-type="aff" rid="af4-ijerph-14-01231">4</xref></contrib><contrib contrib-type="author"><name><surname>Georgina</surname><given-names>Hernandez-Flores</given-names></name><xref ref-type="aff" rid="af3-ijerph-14-01231">3</xref></contrib></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Chong</surname><given-names>Yap-Seng</given-names></name><role>Academic Editor</role></contrib></contrib-group><aff id="af1-ijerph-14-01231"><label>1</label>Public Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>alfredo_celis@yahoo.com</email></aff><aff id="af2-ijerph-14-01231"><label>2</label>Environmental Health Department, University of Guadalajara, Sierra Mojada 950, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>f_lozano_k@hotmail.com</email></aff><aff id="af3-ijerph-14-01231"><label>3</label>Immunology Department, Western Research Biomedical Center (IMSS), Sierra Mojada 800, Colonia Independencia, Guadalajara, Jalisco 44340, Mexico;<email>abravoc@prodigy.net.mx</email> (A.B.-C.);<email>gina.geodic1967@gmail.com</email> (H.-F.G.)</aff><aff id="af4-ijerph-14-01231"><label>4</label>Pediatrics Department, Hospital Angeles del Carmen, Health Services, Tarascos 3473 Interior 240A, Fraccionamiento Monraz, Guadalajara, Jalisco 44670, Mexico;<email>mariana.endoc@gmail.com</email></aff><author-notes><corresp id="c1-ijerph-14-01231"><label>*</label>Correspondence: <email>erksland@hotmail.com</email>; Tel.: +52-33-36-48-62-64</corresp></author-notes><pub-date pub-type="epub"><day>16</day><month>10</month><year>2017</year></pub-date><pub-date pub-type="ppub"><month>10</month><year>2017</year></pub-date><volume>14</volume><issue>10</issue><elocation-id>1231</elocation-id><history><date date-type="received"><day>22</day><month>7</month><year>2017</year></date><date date-type="accepted"><day>11</day><month>10</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 by the authors.</copyright-statement><copyright-year>2017</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><p>The presence of albumin in urine has been used for more than four decades as a marker of renal and cardiovascular damage. Most of the information on this marker is related to adults. The prevalence of albuminuria in the pediatric population has been reported as being 2.2–12.8% in some countries. Most research in this field is related to albuminuria and diseases, such as diabetes and hypertension. Using the methodology described by Arksey and O’Malley in 2005, a scoping review was carried out to show that the presence of albumin in urine in the pediatric population might be associated with environmental, demographic, congenital, infectious, and non-infectious factors. The information collected is supported by 74 references present in PubMed. The results reveal the multiple causes associated with albuminuria in the pediatric population. This information can be very useful for clinical practice by adding knowledge about albuminuria behavior in children.</p></abstract><kwd-group><kwd>albuminuria</kwd><kwd>pediatric population</kwd><kwd>risk factor</kwd></kwd-group></article-meta></front><body><sec id="sec1-ijerph-14-01231"><title>1. Introduction</title><p>At the end of the 1960s, Peterson et al. determined that quantitative analysis of albumin in urine was useful to detect renal alterations [<xref rid="B1-ijerph-14-01231" ref-type="bibr">1</xref>]. Since then, albumin levels in urine have been used clinically as a tool to measure kidney failure in patients with diabetes mellitus and hypertension [<xref rid="B2-ijerph-14-01231" ref-type="bibr">2</xref>,<xref rid="B3-ijerph-14-01231" ref-type="bibr">3</xref>]. Once the relationship between albuminuria and kidney failure was established, quantification methods were developed to be faster and more precise [<xref rid="B4-ijerph-14-01231" ref-type="bibr">4</xref>].</p><p>At present, albuminuria is known as a renal and cardiovascular predictor not only in diabetic patients, but also in those who are apparently healthy. The reported prevalence in general population is 7.2% [<xref rid="B5-ijerph-14-01231" ref-type="bibr">5</xref>]. The majority of studies have been conducted in adults, despite the interest in early detection having risen recently due to future effects. In Japan, this method has been used since 1979 to detect kidney diseases in the pediatric population [<xref rid="B6-ijerph-14-01231" ref-type="bibr">6</xref>]. Other countries, such as Australia, the U.K., Norway, the U.S., and Italy, have also carried out this practice since the mid-1980s [<xref rid="B7-ijerph-14-01231" ref-type="bibr">7</xref>]. Information on prevalence is limited but is reported as approximately 7% [<xref rid="B8-ijerph-14-01231" ref-type="bibr">8</xref>]. Another study reported that the median ACR (albumin/creatinine ratio) of the random morning urine specimen for children <10 years was 2.91 vs. 2.28 mg/g (<italic>p</italic> < 0.001) for children ≥10 years. The median urinary albumin concentration for children <10 years was significantly higher than in children ≥10 years (2.53 vs. 2.09 μg/mL; <italic>p</italic> = 0.008) [<xref rid="B9-ijerph-14-01231" ref-type="bibr">9</xref>]. More recently, an Australian study considered 975 children aged 5–18 years. The overall prevalence of albuminuria, as defined by an ACR greater than 30 mg/g, was 12.8% (95% CI 9.9–15.6). In males, the frequency of albuminuria was 10.2% (95% CI 6.1–14.2) and in females, it was 15.5% (95% CI 10.7–20.3) [<xref rid="B10-ijerph-14-01231" ref-type="bibr">10</xref>].</p><p>Orthostatic proteinuria is the most common cause of a positive result of protein (albumin among the various proteins in urine) in pediatric patients (often tall, physically active adolescents). In this circumstance, the detection of isolated proteinuria (in the absence of hematuria) in an asymptomatic individual based on a random specimen during the day must be confirmed by repeating the test (dipstick) on a specimen collected immediately upon patient’s awakening in the morning [<xref rid="B11-ijerph-14-01231" ref-type="bibr">11</xref>]. In 2010, Brandt et al. characterized the 24-h and diurnal variability of urinary protein excretion and identified the prevalence of orthostatic proteinuria (OP) in healthy children. Upright, supine and 24-h total urinary protein (UrTP) was measured in 91 healthy children aged 6–19 years. The UrTP concentration (mg/dL) was measured using a pyearsocatechol violet method. All participants had normal serum creatinine levels. The mean 24-h UrTP excretion was 64 mg/m<sup>2</sup> (SD 65).</p><p>An elevated 24-h UrTP of >100 mg/m<sup>2</sup> was found in 18 (19.8%) participants. These 18 participants had orthostatic proteinuria. Three participants (3%) had a normal 24-h protein but an elevated supine protein excretion rate (range of 4.1–5.5 mg/m<sup>2</sup>/h), with a mean UrTP of 108 mg (69 mg/m<sup>2</sup>/24 h) Absolute UrTP excretion (mg/24 h) was higher in older compared with younger children (<italic>p</italic> < 0.05) and was higher in boys than girls (<italic>p</italic> < 0.05). This concluded that children with mild, asymptomatic proteinuria should have a first-morning urine UPcr (urinary protein to creatinine ratio) to rule out OP before further testing and consideration of a referral. Children with normal first-morning urinary protein do not require extensive testing for renal disease and can be monitored yearly for evidence of changing urinary protein excretion [<xref rid="B12-ijerph-14-01231" ref-type="bibr">12</xref>].</p><p>Extensive information already exists in the literature related to the relationship between albuminuria and diseases, such as diabetes, hypertension, cardiopathies, human immunodeficiency virus (HIV) infection, as well as different nephropathies in the pediatric population. The aim of the present study was to review all available information related to the relationship between albuminuria and less common risk factors other than those previously mentioned, as well as to discuss to the association of albuminuria with demographic, pathological, and environmental factors. Finally, the purpose was to alert the reader about the vast diversity of factors causing albuminuria, in order for these to be taken into account when applying detection tests in pediatric population.</p></sec><sec id="sec2-ijerph-14-01231"><title>2. Materials and Methods</title><p>The methodology described by Arksey and O’Malley was used [<xref rid="B13-ijerph-14-01231" ref-type="bibr">13</xref>]. First, a question for the literature review was defined and an information search was subsequently initiated, with PubMed being the main index considered. At the beginning, the key words were albuminuria, children, preschool, and risk factors. Notably, when combining such words, many terms related to articles on diabetes appeared. Thus, we employed the Boolean operator “not” before “diabetes” in order to decrease the number of results. <xref ref-type="table" rid="ijerph-14-01231-t001">Table 1</xref> graphically depicts the search strategy and results obtained from PubMed.</p><p>The main reference selection criteria were: English issues, empirical quantitative and pediatric population research. All articles included were full texts. Papers excluded were those related to: diabetes mellitus, systemic arterial hypertension, HIV infection, any stage of chronic kidney failure, common nephropathies, transplanted patients, oncologic diseases studies and hospitalized patients. In addition, reviews and manuscripts with only an abstract were not considered.</p><p>The search, review and selection of papers were performed for eight weeks (September–November 2016) and manuscripts were in the year range of 1981–2016. A total of 74 references were considered (57 for the review and 17, complementary ones). Due to importance of the information, an article published in 2017 was included in the final version of this manuscript.</p><p>The selected manuscripts were analytically systematized in an excerpt matrix to organize them easily. For each article, the excerpt matrix considered the following: main author; country of origin; date; design; sample characteristics; data analysis and results. After all articles were processed, a summary of the results was created, which was gathered according to their etiologic factor. <xref ref-type="table" rid="ijerph-14-01231-t002">Table 2</xref> summarizes the characteristics of the included studies.</p></sec><sec id="sec3-ijerph-14-01231"><title>3. Results</title><sec id="sec3dot1-ijerph-14-01231"><title>3.1. Environmental Factors </title><p>Some children and adolescents are often exposed to environmental factors, which can affect their health in the pediatric stage in addition to having serious consequences later on in the future. Several elements have been reported as being detrimental to people’s health, some of which have been associated with direct kidney damage. Bisphenol A (BPA) is a compound found in products that are consumed daily. Exposure of the pediatric population to this element has been studied for more than a decade [<xref rid="B14-ijerph-14-01231" ref-type="bibr">14</xref>]. By 2011, canned soup was demonstrated to be related with high BPA levels in urine [<xref rid="B15-ijerph-14-01231" ref-type="bibr">15</xref>]. Simultaneously, another study demonstrated the possibility of health damage in the pediatric population due to BPA exposure [<xref rid="B16-ijerph-14-01231" ref-type="bibr">16</xref>]. To date, scientific evidence has demonstrated a relationship between urinary BPA and albuminuria in this population [<xref rid="B17-ijerph-14-01231" ref-type="bibr">17</xref>]. BPA can co-exist with other pollutants, such as phthalates, which have also been shown to be correlate with consumption levels and can be detrimental to one’s health, specifically causing albuminuria [<xref rid="B18-ijerph-14-01231" ref-type="bibr">18</xref>,<xref rid="B19-ijerph-14-01231" ref-type="bibr">19</xref>,<xref rid="B20-ijerph-14-01231" ref-type="bibr">20</xref>].</p><p>Distinct components in the environment (heavy metals) also result in renal toxicity. Lead and cadmium are heavy metals that, together with high- or low-molecular weight proteins, have been associated with albuminuria in pediatric and adult urine [<xref rid="B21-ijerph-14-01231" ref-type="bibr">21</xref>,<xref rid="B22-ijerph-14-01231" ref-type="bibr">22</xref>]. Other molecules, as chromium, arsenic and mercury, have been studied to determine levels of damage to the kidney and their relationships with albuminuria [<xref rid="B23-ijerph-14-01231" ref-type="bibr">23</xref>,<xref rid="B24-ijerph-14-01231" ref-type="bibr">24</xref>]. However, different authors have not found any relationship between albuminuria and such elements in the pediatric population [<xref rid="B25-ijerph-14-01231" ref-type="bibr">25</xref>].</p><p>Cigarette smoke is among pollutants in the environment that are also related to albuminuria in the early stages. In 2007, a study in adults revealed a relationship between smoking and albuminuria [<xref rid="B26-ijerph-14-01231" ref-type="bibr">26</xref>]. In 2013, another study in the pediatric population reported independent associations between chronic kidney disease, smoking and proteinuria [<xref rid="B27-ijerph-14-01231" ref-type="bibr">27</xref>]. At the same time in the U.S., a different group showed a relationship between urinary cotinine and albuminuria in a multi-ethnic study [<xref rid="B28-ijerph-14-01231" ref-type="bibr">28</xref>]. Therefore, there is an important role of pesticide exposure in these situations, even more so in pediatric working populations. The scientific evidence points to an association, probably cyclic, between pesticide exposure (xenobiotics) and nicotine with albuminuria in vulnerable groups [<xref rid="B29-ijerph-14-01231" ref-type="bibr">29</xref>].</p></sec><sec id="sec3dot2-ijerph-14-01231"><title>3.2. Non-Transmissible Diseases</title><p>The relationship between albuminuria and chronic diseases, such as diabetes mellitus and arterial hypertension, has been previously mentioned [<xref rid="B2-ijerph-14-01231" ref-type="bibr">2</xref>,<xref rid="B3-ijerph-14-01231" ref-type="bibr">3</xref>]. However, there are other non-transmissible pathologies related to albuminuria. Sickle-cell anemia is an autosomal recessive disorder associated with chronic kidney disease. Two trials have reported that the prevalence of albuminuria was 15.5–20.7% in separate groups of 90 and 410 pediatric patients, establishing it as an early marker of kidney failure [<xref rid="B30-ijerph-14-01231" ref-type="bibr">30</xref>,<xref rid="B31-ijerph-14-01231" ref-type="bibr">31</xref>]. In 2014, a multi-national study in Africa with 2582 patients with sickle cell disease revealed that the prevalence of albuminuria was 29.2% in general and 27% in children younger than 10 years old [<xref rid="B32-ijerph-14-01231" ref-type="bibr">32</xref>]. The study determined that the frequency of albuminuria varies according to age and country with a higher frequency of 46% in Cameroon (32).</p><p>Some other studies consider obesity as a risk factor for albuminuria. In 2014, a study in 901 children aged 6–16 years, 565 of whom were obese, found no difference in albuminuria levels with or without obesity [<xref rid="B33-ijerph-14-01231" ref-type="bibr">33</xref>]. However, these authors determined that albuminuria was directly related with glomerular filtration rate [<xref rid="B33-ijerph-14-01231" ref-type="bibr">33</xref>]. Additionally, the prevalence of albuminuria in overweight and obese infants has been shown to be 2.7–4%, which does not differ significantly from estimations in the general population [<xref rid="B34-ijerph-14-01231" ref-type="bibr">34</xref>,<xref rid="B35-ijerph-14-01231" ref-type="bibr">35</xref>]. Meanwhile, some other reports indicated that in non-obese adolescents, the prevalence of albuminuria is 8.7% compared to 0.3% in obese adolescents [<xref rid="B36-ijerph-14-01231" ref-type="bibr">36</xref>].</p><p>Respiratory disorders are not excluded as risk factors for albuminuria in the pediatric population. A study conducted in Greece [<xref rid="B37-ijerph-14-01231" ref-type="bibr">37</xref>], reported an association between albuminuria and severe obstructive sleep apnea in children aged 2–14 years, which occurred as a result of hypoxemia (oxidative stress). Congenital hypothyroidism and Kwashiorkor disease have also been studied, although no relationship with albuminuria has been established to the best of our knowledge [<xref rid="B38-ijerph-14-01231" ref-type="bibr">38</xref>,<xref rid="B39-ijerph-14-01231" ref-type="bibr">39</xref>].</p></sec><sec id="sec3dot3-ijerph-14-01231"><title>3.3. Transmissible Diseases</title><p>Some infectious diseases have been related to albuminuria, which are mainly transmitted by parasites, bacteria, and viruses. Regarding parasites, having urogenital infections by <italic>Schistosoma haematobium</italic> is considered as a high risk in African countries, especially in the pediatric population. Several studies have reported that this condition is associated with albuminuria and the albumin/creatinine ratio when comparing frequencies between infected and healthy patients [<xref rid="B40-ijerph-14-01231" ref-type="bibr">40</xref>,<xref rid="B41-ijerph-14-01231" ref-type="bibr">41</xref>,<xref rid="B42-ijerph-14-01231" ref-type="bibr">42</xref>]. Furthermore, this has established it as diagnostic marker for the disease and as a way to monitor early complications, particularly in preschool children. Several studies have related intestinal parasites to chronic and acute renal diseases in infants and adults who had no albuminuria, despite exhibiting abnormalities in the general urine test [<xref rid="B43-ijerph-14-01231" ref-type="bibr">43</xref>,<xref rid="B44-ijerph-14-01231" ref-type="bibr">44</xref>]. In 2014, a study in India included children older than 11 years of age and adults, with the goal of describing with the relationship of renal disease with <italic>Orientia tsutsugamushi</italic> infections [<xref rid="B45-ijerph-14-01231" ref-type="bibr">45</xref>]. Results indicated that 55% of infected patients presented with albuminuria. Moreover, another study in 2010 revealed the association between albuminuria and <italic>Leishmania</italic> infection, with a prevalence of 42% in infected patients [<xref rid="B46-ijerph-14-01231" ref-type="bibr">46</xref>].</p><p>Albuminuria in patients with a urinary tract infection (UTI) has also been studied, which found statistically significant differences in pediatric groups with and without UTI in terms of albuminuria levels and albumin/creatinine ratio [<xref rid="B47-ijerph-14-01231" ref-type="bibr">47</xref>]. Other reports demonstrate an incidence of 51% of albuminuria in pediatric patients with renal scars, secondary to pyelonephritis [<xref rid="B48-ijerph-14-01231" ref-type="bibr">48</xref>]. The authors of reference [<xref rid="B48-ijerph-14-01231" ref-type="bibr">48</xref>] utilized this parameter as a long-standing biologic marker. In 1999, a trial in children aged 1.9–16 years demonstrated an association of albuminuria with recurrent tonsillitis (<italic>Streptococcus pyogenes</italic>), recurrent-hypertrophic tonsillitis and hypertrophic tonsillitis with a prevalence of 50%, 38.5%, and 20% respectively, at the time of the tonsillectomy, before there was a decrease six months after surgery [<xref rid="B49-ijerph-14-01231" ref-type="bibr">49</xref>]. In 2013, an evaluation in Vietnam failed to determine an association of dengue infections and other variables with albuminuria in pediatric patients [<xref rid="B50-ijerph-14-01231" ref-type="bibr">50</xref>]. The prevalence of albuminuria in both groups was 12%.</p></sec><sec id="sec3dot4-ijerph-14-01231"><title>3.4. Uncommon and Congenital Nephropathies Causing Albuminuria</title><p>Hemolytic Uremic Syndrome (HUS) is considered an infectious disease sequalae with potential renal damage. In reports of cases and controls, a frequency of albuminuria of 40% compared to 3.3% albuminuria was found in children with a HUS background and their healthy controls, respectively [<xref rid="B51-ijerph-14-01231" ref-type="bibr">51</xref>]. Likewise, follow-up studies in patients with this background had results evaluated 3–5 years after the outbreak. Albuminuria frequencies in these patients were 32% and 20%, respectively, compared to healthy subjects [<xref rid="B52-ijerph-14-01231" ref-type="bibr">52</xref>,<xref rid="B53-ijerph-14-01231" ref-type="bibr">53</xref>]. Familial Mediterranean Fever (FMF) is an autosomal recessive disease defined by fever episodes, renal polyserositis, and amyloidosis. An experiment with 50 children with FMF and healthy ones measured kidney function in both groups. The authors found a significant difference only in regard to albuminuria and suggested it as a useful monitoring tool in order to decrease future kidney complications [<xref rid="B54-ijerph-14-01231" ref-type="bibr">54</xref>].</p></sec><sec id="sec3dot5-ijerph-14-01231"><title>3.5. Congenital Urinary Tract Malformations </title><p>A solitary functioning kidney is a clear example of renal mass-decrease function in which hyperfiltration consequences could be expected. This fact could be applied to subjects with congenital or acquired solitary functioning kidneys. A research group in 2006 determined the solitary functioning kidney etiology in a group of patients <18 years of age [<xref rid="B55-ijerph-14-01231" ref-type="bibr">55</xref>], which was 49% due to congenital renal agenesis (CRA), 41% secondary to nephrectomy and the remainder due to different causes. In patients with congenital renal agenesis, the average follow-up was 9.1 years. The frequency of albuminuria in all the groups was 12.6%, while it was 31.6% in the congenital renal agenesis group. Finally, in patients with a nephrectomy background, a frequency of 7.9% was found. Studies in cases and controls determined in 2014 that there was no significant difference between glomerular filtration and albuminuria in healthy or in subjects with a solitary functioning kidney. The authors also reported that changes in kidney function and albuminuria are directly related with time and patients with a solitary functioning kidney had a higher hyperperfusion risk [<xref rid="B56-ijerph-14-01231" ref-type="bibr">56</xref>]. Another study tracked a group of 42 children with a solitary functioning kidney for 11.3 years [<xref rid="B57-ijerph-14-01231" ref-type="bibr">57</xref>]. The frequency of albuminuria in 42 of these children was 7.1%, while this frequency was 7.4% and 6.4% for the groups with congenital renal agenesis and a solitary functioning kidney, respectively.</p><p>Autosomal dominant polycystic kidney disease (ADPKD) is one of the most frequent inheritable conditions. In 1998, a report in 189 children of families with this condition revealed that of the 103 of them with ADPKD-positive results, 72% had albuminuria, while in the non-affected group, a frequency of 42% was found [<xref rid="B58-ijerph-14-01231" ref-type="bibr">58</xref>]. In the same year, there was a follow-up study in subjects aged 4–21 years with ADPKD and normal kidney function, in which patients were divided into three groups according to hypertension and ADPKD severity. This study reported an average of 25.3 mcg/day of urinary albumin in the three groups, which did not significantly differ [<xref rid="B59-ijerph-14-01231" ref-type="bibr">59</xref>]. Later, albuminuria was used as an early renal failure marker in children aged 1–17 years as there was a frequency of 58% for albuminuria in the study group [<xref rid="B60-ijerph-14-01231" ref-type="bibr">60</xref>].</p><p>Other congenital entities, such as vesicoureteric reflux (VUR), have also been studied, revealing a direct proportional relationship between albuminuria levels and the degree of nephropathy secondary to VUR [<xref rid="B61-ijerph-14-01231" ref-type="bibr">61</xref>]. A study in 2007 reviewed retrospectively the notes of 176 children born in 1970–1998 that were diagnosed with chronic renal failure (CRF). Seventy-four (42%) children had renal failure secondary to urinary tract obstruction and 102 children (58%) secondary to renal dysplasia alone (<italic>n</italic> = 41) or with VUR (<italic>n</italic> = 61). There was a significant relationship between the amount of albuminuria and the rate of deterioration (<italic>p</italic> < 0.001). Children with ACR <50 mg/mmoL showed a median deterioration of −1.5 mL/min per 1.73 m<sup>2</sup>, whereas children with pronounced proteinuria and ACR of >200 mg/mmoL had a median deterioration of –6.5 mL/min per 1.73 m<sup>2</sup> per year [<xref rid="B62-ijerph-14-01231" ref-type="bibr">62</xref>].</p></sec><sec id="sec3dot6-ijerph-14-01231"><title>3.6. Demographic Factors</title><p>There is evidence related to demographical factors concerning the prevalence of albuminuria according to gender and age [<xref rid="B53-ijerph-14-01231" ref-type="bibr">53</xref>,<xref rid="B63-ijerph-14-01231" ref-type="bibr">63</xref>,<xref rid="B64-ijerph-14-01231" ref-type="bibr">64</xref>,<xref rid="B65-ijerph-14-01231" ref-type="bibr">65</xref>]. Other scientific research considers that even when there are differences regarding gender, age is inversely proportional to albuminuria levels in boys and girls [<xref rid="B66-ijerph-14-01231" ref-type="bibr">66</xref>]. Likewise, there are reports on the prevalence of albuminuria (8.3% vs. 2.1%) in newborn infants with low birth weights when compared to normal-weight newborns [<xref rid="B67-ijerph-14-01231" ref-type="bibr">67</xref>]. Some studies also report a similar albuminuria prevalence in ethnic groups [<xref rid="B66-ijerph-14-01231" ref-type="bibr">66</xref>], even when others show differences in albuminuria levels in Australian aboriginal and non-aboriginal people [<xref rid="B68-ijerph-14-01231" ref-type="bibr">68</xref>]. It is important to emphasize that in the latter study, the difference observed in Australian aboriginal people is associated with obesity, which was already discussed previously. In addition, other studies in Australia also present a prevalence of 7.3% for albuminuria in Australian aboriginal people without any difference in non-aboriginal people. Moreover, these authors indicate that neither place-of-residence, age, gender, nor social conditions are factors affecting the prevalence of albuminuria [<xref rid="B69-ijerph-14-01231" ref-type="bibr">69</xref>].</p></sec></sec><sec id="sec4-ijerph-14-01231"><title>4. Discussion</title><p>Albuminuria is defined as the presence of albumin in urine in a range of 30–300 μg/mg [<xref rid="B70-ijerph-14-01231" ref-type="bibr">70</xref>]. When the urinary albumin level is divided by the urinary creatinine value, the albumin/creatinine ratio is obtained, which is an estimation reported in several studies [<xref rid="B71-ijerph-14-01231" ref-type="bibr">71</xref>]. Thus, by employing both parameters, urinary albumin levels and their frequency can be reported in specific populations. The prevalence and variability of albuminuria have already been mentioned as being related to certain pathologies, such as age, gender, etc. However, it is noteworthy that the determination of urinary albumin also depends on instruments from simple test strips to more modern, sensitive, and easy-to-use methods, particularly in children [<xref rid="B8-ijerph-14-01231" ref-type="bibr">8</xref>,<xref rid="B72-ijerph-14-01231" ref-type="bibr">72</xref>]. Additionally, the human factor may also be considered as strong determinant in results.</p><p>The use of this assay is well established as a screening test in Asian countries, such as Japan, Taiwan, and South Korea. However, this is still global controversy with respect to its use and there is no international consensus, at least in Western countries, related to the benefit of its use in children or adolescents [<xref rid="B73-ijerph-14-01231" ref-type="bibr">73</xref>]. Some other authors consider the use of test strips as an economic, but not-very-helpful, screening tool [<xref rid="B74-ijerph-14-01231" ref-type="bibr">74</xref>].</p><p>In general, and based on the present study, the use of this marker might present several advantages in cardiovascular and early renal conditions. Nevertheless, this is mainly for the populations at risk that are already defined, as it is not clear whether their detection in relatively healthy patients is appropriate when there is a lack of risk factors. Furthermore, among the environmental factors mentioned, including BPA, phthalates and heavy metals, more long-term studies are needed to define their real importance as risk factors. In addition, from this review, the cyclic nature of albuminuria is evident, especially in children. Exposure (even temporary) to risk factors should also be taken into account when testing. Moreover, in terms of the variable nature of this marker, its inversely proportional relationship with age must be added. All these details are relevant when considering that prevalence in chronic kidney disease, with non-diabetic and non-hypertensive patients, does not match with the prevalence of albuminuria in pediatric populations without renal disease.</p></sec><sec id="sec5-ijerph-14-01231"><title>5. Conclusions</title><p>Finally, it is possible to conclude that urinary albumin detection is a useful tool with prognostic value. However, there are some gaps regarding its use in general pediatric population and its role in several diseases is not clear. Changes in the prevalence of albuminuria within a specific place and in the pediatric population could be explained by taking in account several associated factors due to its probable cyclic behavior. Achieving reliable results would depend on diagnostic tests, particular cases and only in massive case detection, controlling, and considering all possibilities affecting the nature of urinary albumin.</p></sec></body><back><ack><title>Acknowledgments</title><p>This work was supported by the Public Health Department of the University of Guadalajara.</p></ack><notes><title>Author Contributions</title><p>All authors participated in the search, selection and analysis of the articles. 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Solid-phase fluorescent immunoassay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Tsai (2016) China [<xref rid="B19-ijerph-14-01231" ref-type="bibr">19</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional analyses</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 184 (<10 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. <break></break>Radioimmunoassay (RIA) using albumin RIA kit</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Trasande (2014) USA [<xref rid="B20-ijerph-14-01231" ref-type="bibr">20</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 667 (6–19 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">First morning urine sample. Solid-phase fluorescent immunoassay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Chan (2012) China [<xref rid="B21-ijerph-14-01231" ref-type="bibr">21</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 3102 (1–21 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. Immunoturbidimetric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Noonan (2002) USA [<xref rid="B22-ijerph-14-01231" ref-type="bibr">22</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Case-control</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 159 (6–17 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. Enzyme immunosorbent assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cardenas (2016) Mexico [<xref rid="B23-ijerph-14-01231" ref-type="bibr">23</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional sampling</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 107 (5–12 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. Turbidimetry method on Radox Daytona</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Kong (2012) China [<xref rid="B25-ijerph-14-01231" ref-type="bibr">25</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 120 (12–19 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Morning urine sample. Immunoturbidimetric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Omologa (2013) USA [<xref rid="B27-ijerph-14-01231" ref-type="bibr">27</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 366 (1–16 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. Method not described</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Nascimento (2017) Brazil [<xref rid="B29-ijerph-14-01231" ref-type="bibr">29</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 66 (6–12 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two urine samples 6 months apart. Immunoturbidimetric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Becton (2010) USA [<xref rid="B30-ijerph-14-01231" ref-type="bibr">30</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 90 (2–18 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two urine samples 6 months apart. Immunoturbidimetric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">McPherson (2011) USA [<xref rid="B31-ijerph-14-01231" ref-type="bibr">31</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 410 (2–21 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. Radioimmunoassay (RIA)</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ranque (2014); five countries in sub-Saharan Africa [<xref rid="B32-ijerph-14-01231" ref-type="bibr">32</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 2582 <break></break>(N = 527 <10 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. HemoCue Albumin 20 system or Siemens Clinitek StatusAnalyzer</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Di Bonito (2014) Italy [<xref rid="B33-ijerph-14-01231" ref-type="bibr">33</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 901 (6–16 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">First morning urine sample. Kinetic nephelometric method.</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lurbe (2013) Spain [<xref rid="B34-ijerph-14-01231" ref-type="bibr">34</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 134 (9–18 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">First morning urine sample. Immunonephelometric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Radhakishun (2013) <break></break>The Netherlands [<xref rid="B35-ijerph-14-01231" ref-type="bibr">35</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 408 (3–19 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Morning urine sample. Immunochemistry system</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Nguyen (2013) USA [<xref rid="B36-ijerph-14-01231" ref-type="bibr">36</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 2515 (12–19 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Morning urine sample. Solid-phase fluorescent immunoassay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Varlami (2013) Greece [<xref rid="B37-ijerph-14-01231" ref-type="bibr">37</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Case-control</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 129 (2–14 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two urine samples: 10 p.m. and 8 a.m. h. Immunonephelometric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Wami (2015) Zimbabwe [<xref rid="B40-ijerph-14-01231" ref-type="bibr">40</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 298 (1–10 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Morning urine sample. Clinitek Microalbumin Reagent Strips</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Stothard (2008) Zanzibar [<xref rid="B41-ijerph-14-01231" ref-type="bibr">41</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 66 (9–15 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mid-morning urine sample. Hemastix_reagent strips and Microalbustix_ reagent strips</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Sousa-Figueiredo (2009) Unguja, Tanzania [<xref rid="B42-ijerph-14-01231" ref-type="bibr">42</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 140 (9–15 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mid-morning urine sample. Albumin-HemoCue photometer</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Elnojomi (2010) Sudan [<xref rid="B46-ijerph-14-01231" ref-type="bibr">46</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 88 (children age not available)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24-h urine sample. Turbidimetric kit and ELISA</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Karlen (1996) Sweden [<xref rid="B48-ijerph-14-01231" ref-type="bibr">48</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 57 (1.7–17.9 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Four urine collection periods lasting 30 min each were obtained in every subject. Solid-phase radioimmunological assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lopez-Gonzalez (1999) Spain [<xref rid="B49-ijerph-14-01231" ref-type="bibr">49</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 90 (1.9–16 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two 24-h urine samples 2 months apart. Laser nephelometry</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Hanh Thien (2013) Vietnam [<xref rid="B50-ijerph-14-01231" ref-type="bibr">50</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Prospective descriptive study</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 429 (5–15 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. ELISA using rabbit anti-human albumin polyclonal antibodies and a human serum albumin standard</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Sharma (2010) Canada [<xref rid="B51-ijerph-14-01231" ref-type="bibr">51</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 48 (3–18 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine samples. Immunoassay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Garg (2005) Canada [<xref rid="B52-ijerph-14-01231" ref-type="bibr">52</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 19 cases (1–5 years) <break></break>N = 38 controls</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. Solid-phase competitive chemiluminescent enzyme immunoassay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Garg (2008) Canada [<xref rid="B53-ijerph-14-01231" ref-type="bibr">53</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 19 cases (4–8 years) <break></break>N = 64 controls</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two-first morning urine samples. <break></break>Image Beckman Coulter immunoassay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ergüven (2008) Turkey [<xref rid="B54-ijerph-14-01231" ref-type="bibr">54</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 50 cases (3–19 years) <break></break>N=20 controls (3–17 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24-h urine sample. Immunoturbidimetric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">De Lucas (2006) Spain [<xref rid="B55-ijerph-14-01231" ref-type="bibr">55</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Prospective</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 95 (1–17 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine samples. Method not described</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Shirzai (2014) Turkey [<xref rid="B56-ijerph-14-01231" ref-type="bibr">56</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 44 cases (6–16 years) <break></break>N = 25 controls (5–10 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24-h urine sample. Nephelometry</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Kolvek (2014) Slovakia [<xref rid="B57-ijerph-14-01231" ref-type="bibr">57</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Prospective follow-up study</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 42 (mean 11.3 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24-h urine sample. Method not described</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Sharp (1998) USA [<xref rid="B58-ijerph-14-01231" ref-type="bibr">58</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 103 cases (mean 11.2 years) <break></break>N = 86 controls (mean 10.6 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. Radioimmunoassay (RIA)</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cadnapaphornchai (2009) USA [<xref rid="B59-ijerph-14-01231" ref-type="bibr">59</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Clinical Trial</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 85 (4–21 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two 24-h urine sample. Method not described</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Selistre (2012) France [<xref rid="B60-ijerph-14-01231" ref-type="bibr">60</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 52 (1–17 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Second-morning urine sample. Nephelometry, BM2</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lama (2003) Italy [<xref rid="B61-ijerph-14-01231" ref-type="bibr">61</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Retrospective</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 100 (mean 11.5 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two 24-h urine samples. Enzyme immunoassay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Gonzalez (2007) England [<xref rid="B62-ijerph-14-01231" ref-type="bibr">62</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Retrospective</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 176 (0–11.9 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample (MNS). Method not described</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Davies (1984) England [<xref rid="B63-ijerph-14-01231" ref-type="bibr">63</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 400 (4–16 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24-h urine sample. ELISA</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Gracchi (2015) The Netherlands [<xref rid="B64-ijerph-14-01231" ref-type="bibr">64</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 1352 (24–60 months)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Pantyliners. Nephelometry</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Wu (2014) China [<xref rid="B65-ijerph-14-01231" ref-type="bibr">65</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 1986 (6–19 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Morning spot urine sample. Immunoturbidimetric assay</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Trachtenberg (2007) USA [<xref rid="B66-ijerph-14-01231" ref-type="bibr">66</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Secondary analysis of a clinical trial</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 534 (6–10 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two urine samples 2 years apart. Nephelometric immunochemical methods</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Kim (2017) Australia [<xref rid="B68-ijerph-14-01231" ref-type="bibr">68</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cohort</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 3418</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spot urine sample. <break></break>Dipstick analysis Siemens Clinitek machine</td></tr><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Haysom (2007) Australia [<xref rid="B69-ijerph-14-01231" ref-type="bibr">69</xref>]</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cross-sectional</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">N = 2266 (4–14.8 years)</td><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Morning urine sample. 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