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Increased mortality from acute liver failure in Mexico
Norberto C. Chávez-Tapia
,
Corresponding author
nchavezt@medicasur.org.mx

Correspondence and reprint request:
, Tonatiuh Barrientos-Gutiérrez**,***, Carlos Manuel Guerrero-López***, Jean Josue Santiago-Hernández*, Nahum Méndez-Sánchez*, Misael Uribe*
* Obesity and Digestive Diseases Unit, Medica Sur Clinic and Foundation, Mexico City, Mexico
** Center for Integrative Approaches to Health Disparities, University of Michigan
*** National Institute of Public Health, Mexico City, Mexico
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Introduction</span><p id="p0005" class="elsevierStylePara elsevierViewall">Acute liver failure &#40;ALF&#41; is an uncommon but life-threatening liver disease&#44; characterized by the presence of acute liver damage&#44; encephalopathy&#44; coagulopathy and jaundice&#46; ALF can be divided in hyperacute &#40;less than seven days from the onset of encephalopathy&#41;&#44; acute &#40;more than eight days&#44; but less than four weeks from the onset of encephalopathy&#41; and subacute &#40;more than four weeks from the onset of encephalopathy&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="p0010" class="elsevierStylePara elsevierViewall">The epidemiology of ALF is heterogeneous&#44; being geographic variations and age the most relevant factors in the pattern of disease etiology&#46; This etio-logical variation could affect the prognosis and therapeutic options&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> ALF is considered a rare disease&#44; with an incidence rate of 10-60 cases per 10&#44;000&#44;000 inhabitants in developed countries&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> The ALF mortality rate fluctuates depending on its severity and on access to liver transplantation&#44; and ranges from 13 to 33&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> ALF has a significant impact on liver transplantation programs&#44; accounting for 9-11&#37; of transplants&#46; Liver transplantation significantly reduces ALF mortality&#44; but access to it is still limited&#46;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> In developed countries&#44; the consumption of acetaminophen and other drugs has overtaken viral infection as the primary cause of ALF&#44; accounting for at least 50&#37; of cases&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> However&#44; in developing countries&#44; information regarding the epidemiology of ALF is scarce&#46; The aim of this study was to analyze the data for ALF from the nationwide statistics registry of Mexico&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Material and Methods</span><p id="p0015" class="elsevierStylePara elsevierViewall">The mortality databases were obtained from the National System of Health Information &#40;available at <a href="http://www.sinais.salud.gob.mx/basesdedatos/index.html">http&#58;&#47;&#47;www&#46;sinais&#46;salud&#46;gob&#46;mx&#47;basesdedatos&#47;index&#46;html</a>&#59; accessed September 2&#44; 2011&#41; for every year from 1998 to 2009&#46; The databases contained all deaths registered in Mexico&#44; coded under the International Classification of Diseases version 10 &#40;ICD-10&#41; for the general cause of death&#44; specific cause of death&#44; place of death&#44; age&#44; sex and other socioeconomic variables&#46; Census data from the National Population Council were used to estimate the Mexican population on July 1 in each year of the period examined&#44; overall and by age groups&#44; sex and region &#40;available at <a href="http://www.conapo.gob.mx">http&#58;&#47;&#47;www&#46;conapo&#46;gob&#46;mx</a>&#59; accessed July 13&#44; 2011&#41;&#46;</p><p id="p0020" class="elsevierStylePara elsevierViewall">The ALF-related deaths were classified into two general types based on the ICD-10 descriptors&#58;</p><p id="p0025" class="elsevierStylePara elsevierViewall"><ul class="elsevierStyleList" id="li0005"><li class="elsevierStyleListItem" id="list0005"><span class="elsevierStyleLabel">&#8226;</span><p id="p0030" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">B-codes&#46;</span> Including deaths caused by B150 &#40;hepatitis A&#44; with hepatic coma&#41;&#46; B160&#44; acute hepatitis B with delta agent&#44; with hepatic coma&#46; B162&#44; acute hepatitis B without delta agent&#44; with hepatic coma&#59; and B190&#44; unspecified viral hepatitis&#44; with hepatic coma&#59; and</p></li><li class="elsevierStyleListItem" id="list0010"><span class="elsevierStyleLabel">&#8226;</span><p id="p0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">K-codes&#46;</span> Including deaths caused by K720 &#40;acute and subacute hepatic failure&#41;&#44; K760 &#40;fatty change in the liver&#44; not otherwise classified&#41;&#44; K762 &#40;central hemorrhagic necrosis of the liver&#41; and K763 &#40;infarction of the liver&#41;&#46;</p></li></ul></p><p id="p0040" class="elsevierStylePara elsevierViewall">The mortality rates were calculated as the number of deaths per 10 million inhabitants per year&#46; The calculated mortality rates were regressed over the calendar year using joinpoint regression to test for changes in mortality trends over time&#46; Briefly&#44; joinpoint regression uses an algorithm that tests whether a multisegmented line is a significantly better fit than a straight or less-segmented line&#44; thus identifying break points in the trend&#44; called joinpoints&#46; Each joinpoint denotes a statistically significant &#40;P &#61; 0&#46;05&#41; change in the trend&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> In our analysis&#44; a maximum of three joinpoints &#40;four line segments&#41; were allowed for each model&#46; The data were analyzed using PASW&#174; &#40;PASW Statistics Version 18&#46;0&#46;9&#44; 2009&#59; IBM&#44; Chicago&#44; IL&#44; USA&#41; and the Joinpoint Regression Program&#44; Version 3&#46;5&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a></p><p id="p0045" class="elsevierStylePara elsevierViewall">Geographic differences in the ALF mortality rates were assessed using the regional divisions of the country proposed by the National Institute of Statistics&#44; Geography and Informatics&#44; as follows&#58;</p><p id="p0050" class="elsevierStylePara elsevierViewall"><ul class="elsevierStyleList" id="li0010"><li class="elsevierStyleListItem" id="list0015"><span class="elsevierStyleLabel">&#8226;</span><p id="p0055" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Zone 1&#46;</span> Guerrero&#44; Oaxaca and Chiapas&#46;</p></li><li class="elsevierStyleListItem" id="list0020"><span class="elsevierStyleLabel">&#8226;</span><p id="p0060" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Zone 2&#46;</span> Campeche&#44; Tabasco&#44; Veracruz&#44; Puebla&#44; Hidalgo and San Luis Potos&#237;&#46;</p></li><li class="elsevierStyleListItem" id="list0025"><span class="elsevierStyleLabel">&#8226;</span><p id="p0065" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Zone 3&#46;</span> Michoac&#225;n&#44; Guanajuato&#44; Zacatecas&#44; Durango and Tlaxcala&#46;</p></li><li class="elsevierStyleListItem" id="list0030"><span class="elsevierStyleLabel">&#8226;</span><p id="p0070" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Zone 4&#46;</span> Morelos&#44; Estado de M&#233;xico&#44; Quer&#233;taro&#44; Nayarit&#44; Colima&#44; Sinaloa&#44; Yucat&#225;n and Quintana Roo&#46;</p></li><li class="elsevierStyleListItem" id="list0035"><span class="elsevierStyleLabel">&#8226;</span><p id="p0075" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Zone 5&#46;</span> Tamaulipas&#44; Chihuahua&#44; Sonora&#44; Baja California and Baja California Sur&#46;</p></li><li class="elsevierStyleListItem" id="list0040"><span class="elsevierStyleLabel">&#8226;</span><p id="p0080" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Zone 6&#46;</span> Nuevo Le&#243;n&#44; Coahuila&#44; Jalisco and Aguascalientes&#59; and</p></li><li class="elsevierStyleListItem" id="list0045"><span class="elsevierStyleLabel">&#8226;</span><p id="p0085" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Zone 7&#46;</span> Mexico City&#46;</p></li></ul></p><p id="p0090" class="elsevierStylePara elsevierViewall">A separate linear regression line was fitted for each zone for the 1998-2006 and 2007-2009 periods to identify differences in the slopes of the ALF mortality rates between periods and regions&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Results</span><p id="p0095" class="elsevierStylePara elsevierViewall">From 1998 to 2009&#44; 2&#44;193 deaths attributable to ALF were reported&#46; From 1998 to 2006&#44; the number of ALF-related deaths remained stable&#44; averaging 137 deaths per year&#46; After 2006&#44; ALF-related deaths from all causes increased steadily&#44; although viral etiologies showed a steeper increase&#44; accounting for the highest number of deaths in 2009 &#40;<a class="elsevierStyleCrossRef" href="#f0005">Figure 1</a>&#41;&#46;</p><elsevierMultimedia ident="f0005"></elsevierMultimedia><p id="p0100" class="elsevierStylePara elsevierViewall">The mortality rates behaved in a similar manner&#46; Deaths classified as K720 showed a twofold increase from 1998 to 2009 &#40;from 9&#46;1 to 18&#46;3 deaths per 10&#44;000&#44;000 inhabitants&#41;&#46; Similarly&#44; K760 showed a 2&#46;3-fold increase for the same period &#40;from 1&#46;67 to 3&#46;81 deaths per 10&#44;000&#44;000 inhabitants&#41; &#40;<a class="elsevierStyleCrossRef" href="#f0010">Figure 2</a>&#41;&#46; A 10-fold increase in deaths was observed from 1998 to 2009 for the B-code etiologies &#40;from 1&#46;8 to 18&#46;1 deaths per 10&#44;000&#44;000 inhabitants&#41;&#46; Overall&#44; ALF-related mortality experienced a threefold increase from 1998 to 2009 &#40;from 13&#46;1 to 40&#46;2 deaths per 10&#44;000&#44;000 habitants&#41;&#46; Higher mortality rates&#44; as well as increased rates over time&#44; were concentrated in the group of patients over 45 years old&#44; particularly after 2006 &#40;<a class="elsevierStyleCrossRef" href="#f0015">Figure 3</a>&#41;&#46; No differences by sex were observed&#46;</p><elsevierMultimedia ident="f0010"></elsevierMultimedia><elsevierMultimedia ident="f0015"></elsevierMultimedia><p id="p0105" class="elsevierStylePara elsevierViewall">The trends in ALF-related mortality displayed important increases after 2006 &#40;<a class="elsevierStyleCrossRef" href="#t0005">Table 1</a>&#41;&#46; Joinpoint analysis revealed that across all regions of Mexico&#44; deaths attributable to viral causes &#40;B-codes&#41; showed an average increase of six deaths per year after 2006 compared with previous years &#40;<a class="elsevierStyleCrossRef" href="#f0020">Figure 4</a>&#41;&#59; the increases were remarkably high for Mexico City &#40;zone 7&#41;&#46; For the K-code deaths&#44; an increase of nine deaths per year was observed after 2007 in zones 1 &#40;Guerrero&#44; Oaxaca and Chiapas&#41; and 6 &#40;Nuevo Le&#243;n&#44; Coahuila&#44; Jalisco and Aguascalientes&#41;&#59; the other zones maintained the same slopes over time&#46;</p><elsevierMultimedia ident="t0005"></elsevierMultimedia><elsevierMultimedia ident="f0020"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Discussion</span><p id="p0110" class="elsevierStylePara elsevierViewall">ALF is a rare but lethal disease with important geographic variations in its etiology and prognosis&#46; To the best of our knowledge&#44; this is the first national analysis of ALF in Latin America&#46; Some reports have previously been published involving pediatric populations&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> and infectious etiologies of ALF&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> We analyzed the records of ALF-related mortality in Mexico for 11 years&#46; The most striking finding was the increase in the number of deaths in the last three years of the period&#46; Mortality increased for all etiologies&#44; but hepatitis-related ALF caused by hepatitis A and B viruses and undetermined viruses showed the largest increases&#46;</p><p id="p0115" class="elsevierStylePara elsevierViewall">Because of the secondary and ecological nature of the present study&#44; we are unable to provide a causal explanation for the increase in ALF mortality&#46; However&#44; some considerations can be examined to help interpret these findings&#46; The incidence of hepatitis infections showed its last peak in Mexico in 1997&#44;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> and has remained steady since then&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> An increase in hepatitis-related ALF mortality with a stable incidence of hepatitis could suggest an increase in lethality&#46; However&#44; the assessment of lethality in this situation is difficult because no information on the time lag between hepatitis onset and ALF development exists&#44; precluding any meaningful statements about lethality&#46; Therefore&#44; the current cases of ALF could reflect the 10-year lag since the 1997 hepatitis peak well as present concurrent development of hepatitis and ALF&#46;</p><p id="p0120" class="elsevierStylePara elsevierViewall">We relied on national records to assess these trends&#44; which are subject to reporting bias and changes in the probability of disease detection arising from changes in access to health care&#46; The simultaneous increase in all etiologies and across sexes suggests an improvement in the registration of ALF patients&#44; probably resulting from improved access to health care&#46; ALF is an expensive disease&#44; requiring relatively advanced technological resources to establish an etiological diagnosis&#46; Mexico has recently undergone an extensive reform in health-care access through Seguro Popular&#44; a subsidized governmental system created to provide access to health care for the previously uninsured population&#46; From 2004 to June 2011&#44; 48&#46;5 million people became affiliated with Seguro Popular&#44; many of whom belong to vulnerable groups &#40;Informe de resultados 2011&#44; available at&#58; <a href="http://www.seguro-popular.gob.mx//images/contenidos/Informes_Resultados/informe_resultados_1sem_2011.pdf">http&#58;&#47;&#47;www&#46;seguro-popular&#46;gob&#46;mx&#47;&#47;images&#47;contenidos&#47;Informes&#95;Resultados&#47;informe&#95;resultados&#95;1sem&#95;2011&#46;pdf</a>&#41;&#46; Because Seguro Popular provides coverage for catastrophic expenses and facilitates access to health care&#44; it is reasonable to expect that previously untreated cases of ALF will now be properly diagnosed and followed up&#46; This could explain the increase in ALF mortality&#44; particularly among the elderly&#46;</p><p id="p0125" class="elsevierStylePara elsevierViewall">Another likely explanation is an increase in the vulnerability of the population infected with hepatitis&#46; It is well known that many populations with a formerly high prevalence of hepatitis A viral infections are moving toward medium prevalence in response to improved sanitation&#46; At the same time&#44; hepatitis infections in adulthood have increased as a result of intravenous drug use and sexual transmission&#44; which are also important risk factors for HIV infection&#44; which is still increasing in Mexico&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> Recently&#44; some reports have shown that a large proportion of the adult population infected with hepatitis is also infected with HIV&#46; The comorbidity of HIV and hepatitis has been linked to worse health outcomes&#44; including mortality&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> Finally&#44; local conditions&#44; such as the rare but still prevalent practice of paying plasma donors&#44; could also contribute to the increase in ALF&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a></p><p id="p0130" class="elsevierStylePara elsevierViewall">It is important to note that there are sociogeographic variations in the main causes of ALF&#46; This joint analysis showed slight temporal and geographic variations&#46; Probably the most relevant is the general increase in B-code disease&#44; but the increase in K-code disease in only zones 1 and 6 is also remarkable&#46; This should encourage local researchers to identify the regional epidemiological characteristics and to develop preventive and therapeutic strategies&#46;</p><p id="p0135" class="elsevierStylePara elsevierViewall">Regardless of the specific causes of the increase&#44; 1&#44;121 ALF-related deaths occurred from 2006 to 2009&#46; During the same period&#44; only 383 patients underwent orthotopic liver transplantation for all causes &#40;available at <a href="http://www.cenatra.salud.gob.mx/interior/trasplante_estadisticas.html">http&#58;&#47;&#47;www&#46;cenatra&#46;salud&#46;gob&#46;mx&#47;interior&#47;trasplante&#95;estadisticas&#46;html</a>&#59; accessed October 1&#44; 2011&#41;&#46; This mismatch highlights the dramatic shortage of organs required to accommodate at least the patients who most urgently require liver transplantation&#46; In the current scenario&#44; the vast majority of patients affected by ALF will succumb to the ominous natural history of the disease&#46; This should encourage the development of alternative stratagems to promote living-donor liver transplantation&#44;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> to improve the management of these patients in critical care units&#44; and to promote research into prognos-tic<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> and therapeutic options&#46;</p><p id="p0140" class="elsevierStylePara elsevierViewall">This study was based on administrative data&#44; and some limitations are intrinsic to this methodology&#46; Moreover&#44; other causes of acute liver failure were not included &#40;e&#46;g&#46;&#44; acetaminophen&#44; autoimmune disease&#44; <span class="elsevierStyleItalic">Amanita phalloides</span> consumption&#41;&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Conclusion</span><p id="p0145" class="elsevierStylePara elsevierViewall">In conclusion&#44; in this study&#44; we have shown an increase in the mortality attributable to ALF in Mexico&#44; which was greater in people older than 45 years&#44; with slight geographic variations&#46; These findings warrant further research to determine the real cause of this increase in ALF-related mortality&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Abbreviations</span><p id="p0150" class="elsevierStylePara elsevierViewall"><ul class="elsevierStyleList" id="li0015"><li class="elsevierStyleListItem" id="list0050"><span class="elsevierStyleLabel">&#8226;</span><p id="p0155" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">ALF&#58;</span> Acute liver failure&#46;</p></li><li class="elsevierStyleListItem" id="list0055"><span class="elsevierStyleLabel">&#8226;</span><p id="p0160" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">ICD-10&#58;</span> International Classification of Diseases version 10&#46;</p></li></ul></p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Financial Support</span><p id="p0165" class="elsevierStylePara elsevierViewall">Partially supported by Medica Sur Clinic &#38; Foundation&#46;</p></span></span>"
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          "titulo" => "Financial Support"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abs0005" class="elsevierStyleSection elsevierViewall"><p id="sp0030" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleBold">Introduction&#46;</span> There is significant geographic variation in the etiology and prognosis of acute liver failure &#40;ALF&#41;&#46; Since&#44; little information is available for Latin America&#46; We analyzed ALF mortality trends in Mexico&#46;</p><p id="sp1025" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleBold">Material and methods&#46;</span> The rates of mortality attributable to ALF were obtained for 1998 to 2009 from the National System of Health Information in Mexico and analyzed according to date&#44; etiology&#44; sex&#44; age and geographic characteristics through graphical assessment and joinpoint regression&#46;</p><p id="sp8030" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleBold">Results&#46;</span> From 1998 to 2009&#44; 2&#44;193 ALF-related deaths were reported&#46; A threefold increase in ALF mortality was observed during the period from 1998 to 2009 &#40;the global mortality rate increased from 13&#46;1 to 40&#46;2 deaths per 10&#44;000&#44;000 inhabitants&#41;&#46; The most significant increase was observed for viral etiologies after 2006&#44; affecting people 45 years old and over&#46;</p><p id="sp9030" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleBold">Conclusion&#46;</span> ALF-related deaths have increased since 2006&#46; Although we cannot speculate on the specific causes of this increase&#44; it may reflect improvements in the access of vulnerable populations to health care&#46;</p></span>"
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          "en" => "<p id="sp0005" class="elsevierStyleSimplePara elsevierViewall">Total deaths attributable to acute liver failure in the 1998-2009 period according to the national registry in Mexico&#46;</p>"
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          "en" => "<p id="sp0010" class="elsevierStyleSimplePara elsevierViewall">Mortality rate from acute liver failure &#40;per 10&#44;000&#44;000 habitants&#41; according to the ICD etiology groups&#46;</p>"
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          "en" => "<p id="sp0015" class="elsevierStyleSimplePara elsevierViewall">Mortality rate from acute liver failure &#40;per 10&#44;000&#44;000 habitants&#41; classified by age&#46;</p>"
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          "en" => "<p id="sp0020" class="elsevierStyleSimplePara elsevierViewall">Mortality rate from acute liver failure &#40;per 10&#44;000&#44;000 habitants&#41; and trends using joinpoint analysis&#46;</p>"
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                  \t\t\t\t  " align="center" valign="middle" scope="col">&#916;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="middle" scope="col">Second segment&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="middle" scope="col">&#916;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
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                  \t\t\t\t  " align="center" valign="middle">5&#46;7&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="middle">2005&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="middle">&#8722;0&#46;14&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">9&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">2007&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">6&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">2006&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="middle">0&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="middle">ND&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="middle">2&#46;4&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="middle">2&#46;4&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="middle">ND&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t  " align="center" valign="middle">&#8722;0&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="middle">4&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">2006&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="middle">3&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">2006&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="middle">ND&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t  " align="center" valign="middle">3&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">2006&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="middle">&#8722;0&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t  " align="center" valign="middle">&#8722;0&#46;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">16&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="middle">2006&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
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ISSN: 16652681
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es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos