Effects of Human Immunodeficiency Virus Infection on Recurrence of Tuberculosis after Rifampin-Based Treatment: An Analytical Review
Identifieur interne : 000C79 ( Istex/Corpus ); précédent : 000C78; suivant : 000C80Effects of Human Immunodeficiency Virus Infection on Recurrence of Tuberculosis after Rifampin-Based Treatment: An Analytical Review
Auteurs : Eline L. Korenromp ; Fabio Scano ; Brian G. Williams ; Christopher Dye ; Paul NunnSource :
- Clinical Infectious Diseases [ 1058-4838 ] ; 2003-07-01.
Abstract
We reviewed 47 prospective studies of recurrence of pulmonary tuberculosis (TB) after cure to assess the influence of human immunodeficiency virus (HIV) infection and rifampin treatment. Multivariate regression revealed that the recurrence rate for HIV-uninfected persons increased with decreasing duration of therapy: it was 1.4 cases per 100 person-years for recipients of ⩾7 months of rifampin therapy and 2.0 and 4.0 cases per 100 person-years for recipients of 5–6 and 2–3 months of rifampin therapy, respectively (trend P =.00014), over a mean follow-up duration of 34 months, at a TB incidence of 250 cases per 100,000 person-years. Relative risks of recurrence associated with HIV infection at these 3 treatment durations were 2.2, 2.1, and 3.4, respectively, with a significant interaction between HIV infection status and treatment duration (P =.025). The recurrence rate increased with the background TB incidence (P =.048), and it decreased over time since completion of treatment in HIV-uninfected but not in HIV-infected patients (overall trend, P =.00008; difference by HIV infection status, P =.025). In countries where HIV infection is endemic, TB recurrence may be reduced by administration of rifampin-based treatment for at least 6 months, in accordance with World Health Organization recommendations.
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DOI: 10.1086/375220
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Korenromp</name><affiliation><mods:affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</mods:affiliation></affiliation></author><author><name sortKey="Scano, Fabio" sort="Scano, Fabio" uniqKey="Scano F" first="Fabio" last="Scano">Fabio Scano</name><affiliation><mods:affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</mods:affiliation></affiliation><affiliation><mods:affiliation>E-mail: scanof@who.int</mods:affiliation></affiliation><affiliation><mods:affiliation>Dr. Fabio Scano, World Health Organization, Communicable Diseases, StopTB Dept., Avenue Appia 20, CH 1211, Geneva 27, Switzerland</mods:affiliation></affiliation><affiliation><mods:affiliation>E-mail: scanof@who.int</mods:affiliation></affiliation></author><author><name sortKey="Williams, Brian G" sort="Williams, Brian G" uniqKey="Williams B" first="Brian G." last="Williams">Brian G. 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Korenromp</name><affiliation><mods:affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</mods:affiliation></affiliation></author><author><name sortKey="Scano, Fabio" sort="Scano, Fabio" uniqKey="Scano F" first="Fabio" last="Scano">Fabio Scano</name><affiliation><mods:affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</mods:affiliation></affiliation><affiliation><mods:affiliation>E-mail: scanof@who.int</mods:affiliation></affiliation><affiliation><mods:affiliation>Dr. Fabio Scano, World Health Organization, Communicable Diseases, StopTB Dept., Avenue Appia 20, CH 1211, Geneva 27, Switzerland</mods:affiliation></affiliation><affiliation><mods:affiliation>E-mail: scanof@who.int</mods:affiliation></affiliation></author><author><name sortKey="Williams, Brian G" sort="Williams, Brian G" uniqKey="Williams B" first="Brian G." last="Williams">Brian G. 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Multivariate regression revealed that the recurrence rate for HIV-uninfected persons increased with decreasing duration of therapy: it was 1.4 cases per 100 person-years for recipients of ⩾7 months of rifampin therapy and 2.0 and 4.0 cases per 100 person-years for recipients of 5–6 and 2–3 months of rifampin therapy, respectively (trend P =.00014), over a mean follow-up duration of 34 months, at a TB incidence of 250 cases per 100,000 person-years. Relative risks of recurrence associated with HIV infection at these 3 treatment durations were 2.2, 2.1, and 3.4, respectively, with a significant interaction between HIV infection status and treatment duration (P =.025). The recurrence rate increased with the background TB incidence (P =.048), and it decreased over time since completion of treatment in HIV-uninfected but not in HIV-infected patients (overall trend, P =.00008; difference by HIV infection status, P =.025). In countries where HIV infection is endemic, TB recurrence may be reduced by administration of rifampin-based treatment for at least 6 months, in accordance with World Health Organization recommendations.</div></front></TEI><istex><corpusName>oup</corpusName><author><json:item><name>Eline L. Korenromp</name><affiliations><json:string>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</json:string></affiliations></json:item><json:item><name>Fabio Scano</name><affiliations><json:string>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</json:string><json:string>E-mail: scanof@who.int</json:string></affiliations></json:item><json:item><name>Brian G. 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Multivariate regression revealed that the recurrence rate for HIV-uninfected persons increased with decreasing duration of therapy: it was 1.4 cases per 100 person-years for recipients of ⩾7 months of rifampin therapy and 2.0 and 4.0 cases per 100 person-years for recipients of 5–6 and 2–3 months of rifampin therapy, respectively (trend P =.00014), over a mean follow-up duration of 34 months, at a TB incidence of 250 cases per 100,000 person-years. Relative risks of recurrence associated with HIV infection at these 3 treatment durations were 2.2, 2.1, and 3.4, respectively, with a significant interaction between HIV infection status and treatment duration (P =.025). The recurrence rate increased with the background TB incidence (P =.048), and it decreased over time since completion of treatment in HIV-uninfected but not in HIV-infected patients (overall trend, P =.00008; difference by HIV infection status, P =.025). In countries where HIV infection is endemic, TB recurrence may be reduced by administration of rifampin-based treatment for at least 6 months, in accordance with World Health Organization recommendations.</p></abstract></profileDesc><revisionDesc><change when="2003-07-01">Published</change></revisionDesc></teiHeader></istex:fulltextTEI><json:item><extension>txt</extension><original>false</original><mimetype>text/plain</mimetype><uri>https://api.istex.fr/document/280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D/fulltext/txt</uri></json:item></fulltext><metadata><istex:metadataXml wicri:clean="corpus oup, element #text not found" wicri:toSee="no header"><istex:xmlDeclaration>version="1.0"</istex:xmlDeclaration><istex:docType PUBLIC="-//NLM//DTD Journal Publishing DTD v2.3 20070202//EN" URI="journalpublishing.dtd" name="istex:docType"></istex:docType><istex:document><article article-type="research-article">
<front>
<journal-meta>
<journal-id journal-id-type="hwp">cid</journal-id>
<journal-id journal-id-type="publisher-id">cid</journal-id>
<journal-title>Clinical Infectious Diseases</journal-title>
<abbrev-journal-title>Clinical Infectious Diseases</abbrev-journal-title>
<issn pub-type="ppub">1058-4838</issn>
<issn pub-type="epub">1537-6591</issn>
<publisher>
<publisher-name>The University of Chicago Press</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.1086/375220</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>HIV/AIDS</subject>
<subj-group subj-group-type="heading">
<subject>Major Articles</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Effects of Human Immunodeficiency Virus Infection on Recurrence of Tuberculosis after Rifampin-Based Treatment: An Analytical Review</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Korenromp</surname>
<given-names>Eline L.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Scano</surname>
<given-names>Fabio</given-names>
</name>
<xref rid="cor1" ref-type="corresp"></xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Williams</surname>
<given-names>Brian G.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dye</surname>
<given-names>Christopher</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nunn</surname>
<given-names>Paul</given-names>
</name>
</contrib>
<aff id="aff1"><label>1</label><institution>Communicable Diseases, Stop TB Department, World Health Organization</institution>, <addr-line>Geneva, Switzerland</addr-line></aff>
</contrib-group>
<author-notes>
<corresp id="cor1">Dr. Fabio Scano, World Health Organization, Communicable Diseases, StopTB Dept., Avenue Appia 20, CH 1211, Geneva 27, Switzerland (<email>scanof@who.int</email>).</corresp>
</author-notes>
<pub-date pub-type="ppub">
<day>1</day>
<month>7</month>
<year>2003</year>
</pub-date>
<volume>37</volume>
<issue>1</issue>
<fpage>101</fpage>
<lpage>112</lpage>
<history>
<date date-type="received">
<day>6</day>
<month>9</month>
<year>2002</year>
</date>
<date date-type="accepted">
<day>3</day>
<month>3</month>
<year>2003</year>
</date>
</history>
<copyright-statement>© 2003 by the Infectious Diseases Society of America</copyright-statement>
<copyright-year>2003</copyright-year>
<abstract>
<p>We reviewed 47 prospective studies of recurrence of pulmonary tuberculosis (TB) after cure to assess the influence of human immunodeficiency virus (HIV) infection and rifampin treatment. Multivariate regression revealed that the recurrence rate for HIV-uninfected persons increased with decreasing duration of therapy: it was 1.4 cases per 100 person-years for recipients of ⩾7 months of rifampin therapy and 2.0 and 4.0 cases per 100 person-years for recipients of 5–6 and 2–3 months of rifampin therapy, respectively (trend <italic>P</italic> =.00014), over a mean follow-up duration of 34 months, at a TB incidence of 250 cases per 100,000 person-years. Relative risks of recurrence associated with HIV infection at these 3 treatment durations were 2.2, 2.1, and 3.4, respectively, with a significant interaction between HIV infection status and treatment duration (<italic>P</italic> =.025). The recurrence rate increased with the background TB incidence (<italic>P</italic> =.048), and it decreased over time since completion of treatment in HIV-uninfected but not in HIV-infected patients (overall trend, <italic>P</italic> =.00008; difference by HIV infection status, <italic>P</italic> =.025). In countries where HIV infection is endemic, TB recurrence may be reduced by administration of rifampin-based treatment for at least 6 months, in accordance with World Health Organization recommendations.</p>
</abstract>
</article-meta>
</front>
<body>
<p>Recent observations from countries where HIV infection and tuberculosis (TB) are endemic [<xref rid="ref1" ref-type="bibr">1</xref>] suggest that rates of TB recurrence after completion of treatment may be unacceptably high in HIV-infected patients, even when the DOTS strategy recommended by the World Health Organization (WHO) [<xref rid="ref2" ref-type="bibr">2</xref>] is followed. It is unknown whether the additional recurrences in HIV-infected patients reflect endogenous reactivation involving the original strain (i.e., true relapse), an increased risk of disease after exogenous reinfection with a new TB strain (hereafter known as“reinfection”), or both [<xref rid="ref3" ref-type="bibr">3</xref>]. Therefore, the implications of these high recurrence risks for TB-control policies remain unclear. If relapse is the dominant cause of recurrence, then prolonging first-episode treatment should be considered for TB control. If reinfection is the major cause of recurrence, on the other hand, it may imply a need for posttreatment preventive therapy [<xref rid="ref4" ref-type="bibr">4</xref>, <xref rid="ref5" ref-type="bibr">5</xref>].</p>
<p>The relative rate and the cause of recurrence are likely to vary geographically and over time. Relapse rates depend on treatment efficacy, program quality, and the patients' compliance with therapy. The rate of disease due to reinfection, on the other hand, will be determined mainly by the level of TB exposure and transmission in the population [<xref rid="ref6" ref-type="bibr">6</xref>]. Both are affected by the immunological status of the patients, including HIV infection/AIDS status.</p>
<p>On the basis of indirect evidence, it has generally been accepted that most recurrences of TB represent relapse [<xref rid="ref4" ref-type="bibr">4</xref>, <xref rid="ref7" ref-type="bibr">7</xref>, <xref rid="ref8" ref-type="bibr">8</xref>]. The technique of restriction fragment-length polymorphism (RFLP) analysis now allows us to distinguish between reinfection and relapse as the cause of recurrence. In developing countries, studies that use this technique have mainly found evidence of a high proportion of reinfections among recurrences (e.g., among HIV-infected patients in Nairobi, Kenya [<xref rid="ref9" ref-type="bibr">9</xref>, <xref rid="ref10" ref-type="bibr">10</xref>], and among HIV-uninfected patients in Cape Town, South Africa [<xref rid="ref11" ref-type="bibr">11</xref>]), which seems to be consistent with the high incidence of TB in these populations. Furthermore, among South African mine workers, HIV infection was associated with a 19-fold increase in the incidence of TB disease after reinfection, without an increase in the rate of relapse [<xref rid="ref1" ref-type="bibr">1</xref>].</p>
<p>Because of their small sample sizes and geographical specifics, none of these studies provide, on their own, a definitive answer to questions about the determinants of recurrence rates and causes of recurrence. We report a quantitative synthesis of data from across the world on rates of recurrence, reinfection, and relapse of TB in HIV-infected and HIV-uninfected patients with TB. We investigated the effect of the duration of rifampin treatment, because the WHO recommends rifampin-based treatment in the DOTS strategy for new, drug-susceptible cases (3–4 drugs, including rifampin, for 2 months, followed by 4 months of a regimen containing rifampin or 6 months of therapy with isoniazid and ethambutol [<xref rid="ref2" ref-type="bibr">2</xref>]). The dependence of these outcomes on local TB epidemiology is explored, and the implications for TB treatment regimens in countries where HIV infection is endemic are discussed.</p>
<sec sec-type="methods" id="sec1">
<title>Methods</title>
<p>We reviewed cohort studies on the recurrence of pulmonary TB after receipt of rifampin-based treatment. Studies published up to May 2002 were identified through a search of the PubMed database using the search term(s) “(Mycobacterium) tuberculosis” with the textword “(Recurr* or Relaps* or Reinfect*),” in combination with any of the following Thesaurus terms: “Antitubercular Agents/*therapeutic use,” “Rifampin,” “HIV Infections,” “HIV Seropositivity,” “AIDS-Related Opportunistic Infections/complications,” and “Polymorphism, Restriction Length Fragment.” We also back-traced references from eligible recent studies and the suggestions of experts.</p>
<p>Inclusion criteria were as follows: the study had a duration of follow-up of ⩾6 months after the end of a complete course of treatment; the study subjects (age, >15 years) had a history of smear- or culture-positive pulmonary TB that was cured at the end of treatment, as defined by the completion of a full course of treatment and as demonstrated by negative results of cultures and/or smears (also included were 3 studies in which >80% of patients were smear- or culture-positive for pulmonary TB [<xref rid="ref12" ref-type="bibr">12</xref>–<xref rid="ref14" ref-type="bibr">14</xref>]); the study subjects received treatment with a combination of ⩾2 drugs for 5–12 months, starting with a minimum of 2 months of therapy with rifampin plus ⩾2 other drugs, administered at least twice per week; and recurrences of TB were defined by renewed culture and/or smear positivity after a negative culture at the time of completion treatment.</p>
<p>Eligible studies were cross-referenced to check for overlap. If there were multiple reports about the same group of patients, the study was included only once, although information was sometimes derived from multiple reports.</p>
<p>We recorded sample sizes, durations of follow-up, treatment regimens, recurrence rates, and times to recurrence, by HIV infection status. For studies performed before 1986 in which the patients' HIV infection status was not reported, we assumed that all patients were HIV uninfected. The durations of rifampin regimens were categorized as ⩾7 months, 5–6 months, and 2–3 months; no single study used 4 months of rifampin treatment. Data on follow-up during posttreatment ("secondary") prophylaxis were excluded. However, when studies reported in part on eligible patients (e.g., data on the placebo arm in trials of posttreatment isoniazid prophylaxis), these data were included. The incidence of TB in each country of study (the “background incidence”) was derived from estimates for 1999 [<xref rid="ref15" ref-type="bibr">15</xref>]; for studies from 1980–1998, we assumed the incidence to have followed the time trend of case notifications [<xref rid="ref16" ref-type="bibr">16</xref>]; for studies from before 1980, the estimate for 1980 was used.</p>
<p>Determinants of the recurrence rate were analyzed using least-square multivariate linear regression in SPSS software, version 10.0.7 (SPSS), in which HIV infection status and treatment duration were categorical variables, and TB incidence and follow-up duration were continuous covariates. Studies were weighted in proportion to sample size.</p>
<p>Time patterns in recurrences were assessed by fitting Weibull survivorship functions to the rates of recurrence reported for specific time intervals (between times t<sub>1</sub> and t<sub>2</sub>, which is denoted W[t<sub>1</sub>] - W[t<sub>2</sub>]). If occurrences were said to have occurred at a specific month, we set the time interval to 1 month. The probability of not experiencing a recurrence before time t then is <italic>W</italic>(t) = <italic>e</italic>, where the parameter <italic>α</italic> determines the average recurrence rate and <italic>β</italic> the distribution of recurrences over time. Values for the 2 parameters were maximum likelihood estimates using exact binomial errors.</p>
<p>Finally, we reviewed RFLP studies of the cause of TB recurrences, as defined above. Differing DNA fingerprint patterns between 2 successive cases of TB in one patient were taken to indicate reinfection, and identical fingerprints were taken to indicate relapse, according to the study's interpretation. Because of the small number of RFLP studies, we also included those that reported paired episodes that were identified retrospectively, as well as those that reported recurrences after treatment that had been curative but that did not involve rifampin or for which the total duration of treatment was <5 months. Dependence of the cause of recurrence on the patients' HIV infection status and background TB incidence was investigated by multivariate regression, as specified above.</p>
</sec>
<sec sec-type="results" id="sec2">
<title>Results</title>
<p><bold><italic>Determinants of recurrence rates and cause</italic></bold>. Forty-seven studies provided information on recurrence rates, of which 21 included HIV-infected patients and 41 included HIV-uninfected patients (<xref rid="tab1" ref-type="table">table 1</xref>). The median duration of follow-up was similar for HIV-infected and HIV-uninfected patients, at an average across studies of 27.8 and 36.0 months, respectively (<xref rid="tab2" ref-type="table">table 2</xref>). During this period, a total of 7.0% of HIV-infected patients and 4.2% of HIV-uninfected patients experienced a recurrence of TB. The mean observed recurrence rates were 4.5 and 1.9 cases per 100 person-years in HIV-infected and HIV-uninfected patients, respectively (<italic>P</italic> <.0001). Studies involving HIV-infected and HIV-uninfected patients also differed in the duration of rifampin treatment, which was longer for patients with HIV infection. Also, they tended to differ with regard to the background incidence of TB, which was generally higher in studies that included patients with HIV infection.</p>
<p>Multivariate analysis showed that the recurrence rate significantly decreased with increasing duration of follow-up (<italic>P</italic> <.0001) and with increasing duration of rifampin treatment (<italic>P</italic> =.0001). A high background TB incidence increased recurrence risks by 0.14 cases per 100 person-years for every increase in the TB incidence of 100 cases per 100,000 person-years (<italic>P</italic> =.048). For HIV-uninfected patients treated with a rifampin-based regimen for 5–6 months, this trend translates into a difference in the recurrence rate over 3 years ranging from 1.66 cases per 100 person-years for countries with a low incidence of TB (i.e., 10 cases per 100,000 person-years) to 2.5 cases per 100 person-years for countries with a high incidence of TB (i.e., 600 cases per 100,000 person-years).</p>
<p><xref rid="fig1" ref-type="fig">figure 1</xref> shows the estimated recurrence rates for HIV-infected and HIV-uninfected patients with different treatment durations, at a duration of follow-up of 34 months and an incidence of TB of 250 cases per 100,000 person-years. A large and significant difference appeared between treatment with 2–3 months of rifampin and longer treatment durations (<italic>P</italic> =.0002 for 2–3 months vs. 5–6 months; <italic>P</italic> <.0001 for 2–3 months vs. ⩾7 months). Prolongation of rifampin treatment from 5–6 months to ⩾7 months led to no significant further decrease in recurrence of TB (<italic>P</italic> =.17). For HIV-uninfected persons, the recurrence rate increased with deceasing duration of therapy: it was 1.4 cases per 100 person-years for recipients of ⩾7 months of rifampin therapy and 2.0 and 4.0 cases per 100 person-years for recipients of 5–6 and 2–3 months of rifampin therapy, respectively (overall trend, <italic>P</italic> =.00014), for a mean follow-up duration of 34 months, at a TB incidence of 250 cases per 100,000 person-years. Furthermore, the effect of duration of rifampin treatment was significantly more pronounced in HIV-infected patients than in HIV-uninfected patients (interaction <italic>P</italic> =.025), resulting in relative risks (RRs) of recurrence in HIV-infected versus HIV-uninfected patients of 2.2 (95% CI, 0–4.7) for ⩾7 months of rifampin; 2.1 (95% CI, 1.2–3.1), for 5–6 months; and 3.4 (95% CI, 1.4–5.5), for 2–3 months. For HIV-infected patients alone, the RR of recurrence for treatment durations of 2–3 months versus 5–6 months was 3.2 (95% CI, 1.6–4.7), and the RR for treatment durations of 2–3 months versus ⩾7 months was 4.6 (95% CI, 1.7–7.4).</p>
<p><bold><italic>Relapse versus reinfection</italic></bold>. Sixteen studies reported on rates or proportions of relapse as distinct from reinfection. Overall, 30% of recurrences were due to reinfection. This proportion was 38% among HIV-infected patients and 23% among HIV-uninfected patients (<xref rid="tab2" ref-type="table">table 2</xref>), but the difference was not significant (RR, 1.6; 95% CI, 0.4–2.9). In bivariate analysis, the proportion of recurrences that were due to reinfection tended to increase with background TB incidence (e.g., from 19% at a TB incidence of 10 cases per 100,000 person-years to 31% at an incidence of 600 cases per 100,000 person-years; <italic>P</italic> =.084) but not with the incidence of HIV infection (<italic>P</italic> =.29).</p>
<p><bold><italic>Time patterns in recurrences</italic></bold>. To explain why the duration of follow-up was inversely related to average recurrence rates on regression analysis, <xref rid="fig1" ref-type="fig">figure 1</xref> shows the rates of recurrence over specific time intervals. For HIV-uninfected patients, the recurrence rate decreased rapidly over time during the first 10 months after the completion of treatment and subsequently levelled off, from ∼6 cases per 100 person-years at 1 month to ∼1 case per 100 person-years at 30 months (<xref rid="fig1" ref-type="fig">figure 1</xref> <italic>top</italic>), as would be expected if most recurrences are due to relapse. In contrast, for HIV-infected patients (<xref rid="fig1" ref-type="fig">figure 1</xref>, <italic>bottom</italic>), no difference was detected in the recurrence rates over time. This lack of a time pattern may be related to the larger proportion of recurrences that are due to reinfection in HIV-infected patients. The best-fitting time curves for HIV-infected patients and HIV-uninfected patients differed significantly (<italic>P</italic> =.012). Despite this difference, the median times to recurrence across all studies that reported this were similar (9.7 months [95% CI, 4.9–14 months] for HIV-infected patients and 7.1 months [95% CI, 4.0–10 months] for HIV-uninfected patients; <italic>P</italic> =.37), owing to the higher overall recurrence rate for HIV-infected patients.</p>
<p>For relapse and reinfection, the median reported intervals after the end of treatment were 8.0 months (95% CI, 2.0–14 months) and 16.4 months (95% CI, 8.2–25 months), respectively, for HIV-infected and HIV-uninfected patients combined (<italic>P</italic> =.095). A precise assessment of these time patterns was not possible, because only 3 of the studies that distinguished the causes of recurrence were prospective, and these studies involved small numbers of events [<xref rid="ref1" ref-type="bibr">1</xref>, <xref rid="ref40" ref-type="bibr">40</xref>, <xref rid="ref41" ref-type="bibr">41</xref>].</p>
</sec>
<sec sec-type="discussion" id="sec3">
<title>Discussion</title>
<p>In this review of studies conducted during 1970–1999, HIV infection and a short duration of rifampin treatment independently increased the risk of recurrence of TB. The additional risk incurred by HIV infection was large, especially in association with short durations of rifampin treatment (for regimens including <3 months of rifampin therapy, the RR was 3.4 [95% CI, 1.4–5.4]; <xref rid="fig1" ref-type="fig">figure 1</xref>).</p>
<p>The demonstrated benefit of providing at least 6 months of rifampin therapy is in line with the OR for recurrence after a total treatment duration of 2 months versus a duration of ⩾6 months, which was found to be 6.1 (95% CI, 2.1–17) in a recent meta-analysis of randomized trials on treatment duration (mainly from countries with low prevalences of HIV infection) [<xref rid="ref73" ref-type="bibr">73</xref>]. The stronger effect emerging from that analysis, compared with ours, may relate to its limitation to the first year after treatment—during which proportionally more recurrences are probably due to relapse—and to the inclusion of regimens that did not contain rifampin.</p>
<p>The dependence of recurrence rates on treatment duration suggests that a large proportion of the recurrences in these studies are due to relapse, in both HIV-infected and HIV-uninfected patients. The finding that 70% of recurrences in the subset of RFLP studies were due to relapse is consistent with this finding. With an overall 30% of recurrences still being due to reinfection, the effect of treatment duration on the rate of relapse, specifically, must be even stronger than that shown for the rate of all recurrences of TB (<xref rid="fig1" ref-type="fig">figure 1</xref>).</p>
<p>High background TB incidence increased the recurrence rate considerably; statistically, however, this effect was just marginally significant (<italic>P</italic> =.048). The low significance probably relates to the high proportion of recurrences that were due to relapse, whereas the background incidence would influence only the rate of reinfection. In addition, the country-based estimates of TB incidence may not have been appropriate for all patient populations. For example, the incidence of 8 cases per 100,000 person-years estimated for the United States as a whole [<xref rid="ref16" ref-type="bibr">16</xref>] is possibly too low to represent the populations of urban drug users among whom most TB cases in the US recurrence studies originate. The estimates for earlier years, especially the years before 1980, were crude, in any case, and may, through misclassification, have diluted the observed association. Given that the true effect of background TB incidence may thus be stronger than that estimated here, recurrence rates and the share of reinfection among recurrences are likely to increase to more than the present levels as the incidence of HIV-related TB continues to increase.</p>
<p>Presented estimates are subject to several potential biases. Limiting inclusion to studies in which patients were culture or smear positive for TB may have led to an underestimation of the effect of HIV infection. Because late-stage HIV infection/AIDS is associated with smear negativity [<xref rid="ref74" ref-type="bibr">74</xref>], these studies may have undersampled the patients who had more advanced HIV disease. For HIV-infected patients treated with a 2–3-month course of rifampin, there was only one study available [<xref rid="ref14" ref-type="bibr">14</xref>], and this study, in contrast, included smear-negative patients only. This may have led to an overestimation of the recurrence rate for HIV-infected patients receiving the 2–3-month rifampin regimen specifically, although the estimation for this group—as for all groups—took into account the overall pattern of effects of HIV infection status and treatment duration across all studies. To investigate this potential bias further, we repeated the analysis without including this study. The overall pattern of effects of HIV infection (<italic>P</italic> =.002) and duration of rifampin treatment (<italic>P</italic> =.059) remained the same, but the interaction term between HIV infection status and treatment duration was no longer significant. The highest recurrence rate was still predicted to be among HIV-infected patients treated with rifampin for 2–3 months. Counteracting this potential bias, the majority of other reviewed studies included only patients with new, previously untreated, drug-susceptible TB, which may have led to an underestimation of the effects of HIV infection across all treatment groups as well as of the overall recurrence rates.</p>
<p>The upward bias in recurrence rates may have been enhanced by our ignorance of data on (selective) loss to follow-up and death. Some studies reported rates of loss to follow-up of up to 20% of patients by the third year, but others did not specify the size of the loss, or the specifications involved poorly comparable units (<xref rid="tab1" ref-type="table">table 1</xref>), which were accounted for in variable ways in reported recurrence rates. Follow-up may have been shorter for the sickest patients, because it is, on average, shorter for HIV-infected patients than for HIV-uninfected patients (<xref rid="tab1" ref-type="table">table 1</xref> and <xref rid="tab2" ref-type="table">table 2</xref>). For example, in a cohort in Mexico, all HIV-infected patients died, and relapses were recorded only for HIV-uninfected patients [<xref rid="ref33" ref-type="bibr">33</xref>]; causes of death were not reported, but they may have involved recurrent TB.</p>
<p>Furthermore, meta-analyses of determinants of TB recurrence rates may be prone to publication bias. Our analysis of the influence of HIV infection status at different treatment durations is, however, unlikely to be affected by a publication bias, because the included studies each focused only on subsets of the interaction of interest here. For example, studies compared 2 treatment regimens <italic>or</italic> the influence of HIV infection status for one given treatment regimen (<xref rid="tab1" ref-type="table">table 1</xref>).</p>
<p>Available data did not allow us to evaluate population-specific determinants other than background TB incidence, such as the stage of the HIV epidemic or the local quality of health care, or aspects of the patient mix, such as patient age, patient sex, or the proportion of patients who were smear positive. We cannot exclude the possibility that recurrence risks also depend on such unmeasured factors. However, even if the data had been available to consider such additional variables, the limited statistical power of the analysis would likely preclude any conclusions, because the presented model did already not differ significantly from the data (<italic>P</italic> =.63, by goodness-of-fit statistic). Of equal importance, the effects of TB background incidence that we demonstrated may be confounded with other setting-dependent characteristics. Of note, in countries with a high incidence of TB, the HIV epidemic is usually more advanced, so that HIV-infected patients are, on average, in a later stage of HIV disease and might be even more susceptible to recurrence of TB. Additional analysis, however, revealed that the level of development of the country of study had no significant independent influence on recurrence rates (<italic>P</italic> =.49; Africa, Central and South America, and all Asian countries [except Hong Kong, Singapore, and Thailand, which were excluded] were classified as “developing,” and North American and European countries [except Poland, which was excluded from this part of the analysis] were classified as “developed”).</p>
<p>Despite possible underestimation, the recurrence estimates are on the high side compared with the percentage of treatments (typically 5% [<xref rid="ref75" ref-type="bibr">75</xref>]) coded as “re-treatments” in African TB-control programs. For example, for a country with a background incidence of TB of 400 cases per 100,000 person-years, where one-half of patients with new TB have HIV infection, and where the treatment regimen consists of 5–6 months of rifampin therapy, we would estimate that the recurrence rate is 3.3 cases per 100 person-years. This rate amounts to 9% of the patients >3 years after treatment, and it possibly amounts to an even higher total if recurrences continue to occur at a significant rate thereafter (<xref rid="fig1" ref-type="fig">figure 1</xref>, <italic>bottom</italic>). An explanation may be that TB programs underregister cases involving re-treatment. In Malawi, inspection of program data revealed that >6% of cases registered as new were in fact recurrent, bringing the total percentage of recurrences to ∼10% [<xref rid="ref75" ref-type="bibr">75</xref>].</p>
<p>Findings from the RFLP studies were less conclusive, and the effects of HIV infection on reinfection and relapse rates remain to be determined. There were few such studies; their sample sizes were small, most were not prospective, and the data did not allow consideration of the influence of duration of treatment. Moreover, the interpretation of RFLP fingerprint patterns, with differences denoting reinfection and identical patterns denoting relapse, is subject to debate. Differing fingerprint patterns may alternatively result from mutations within a relapsing strain or falsely appear to be due to sample cross-contamination or mislabeling [<xref rid="ref42" ref-type="bibr">42</xref>, <xref rid="ref67" ref-type="bibr">67</xref>, <xref rid="ref76" ref-type="bibr">76</xref>]. Laboratory artefacts were recently found to be a significant source of differing RFLP fingerprint patterns in a TB research unit in Kampala, Uganda [<xref rid="ref76" ref-type="bibr">76</xref>]. This may explain why a study in Hong Kong found an equal proportion (12%) of differing RFLP fingerprint patterns among subsequent TB episodes and among paired isolates from within a single episode, even after exclusion of isolated positive cultures [<xref rid="ref42" ref-type="bibr">42</xref>]. Of the RFLP studies included in our meta-analysis, only a minority had analyzed isolated positive culture results, as opposed to recurrences defined by multiple cultures [<xref rid="ref40" ref-type="bibr">40</xref>, <xref rid="ref41" ref-type="bibr">41</xref>, <xref rid="ref58" ref-type="bibr">58</xref>, <xref rid="ref60" ref-type="bibr">60</xref>, <xref rid="ref64" ref-type="bibr">64</xref>, <xref rid="ref68" ref-type="bibr">68</xref>], and these studies did not report higher proportions of reinfection. If laboratory artefacts are more common in developing countries, however, laboratory artefacts may have contributed to the contrast in the proportion of cases of reinfection between HIV-infected and HIV-uninfected patients. Furthermore, proportions of cases of reinfection may be inflated by publication bias, because the phenomenon of reinfection has recently received renewed attention. Counteracting these upward biases is the occurrence of reinfection with the same strain, which (like laboratory artefacts) may also be relatively frequent in high-transmission settings.</p>
<p>The single available prospective RFLP study that directly compared HIV-infected and HIV-uninfected patients found that HIV infection increased the rate of TB recurrence due to reinfection by 19-fold without increasing relapse rates, corresponding to proportions of recurrences due to reinfection of 62% in HIV-infected patients and 6% in HIV-uninfected patients [<xref rid="ref1" ref-type="bibr">1</xref>]. However, the generalizability of this study, which was conducted in a South African mining community, is unclear. Not only is the rate of TB exposure unusually high among mining workforces, but miners' susceptibility to recurrence is probably exceptionally high because of occupational risk factors, such as silicosis [<xref rid="ref17" ref-type="bibr">17</xref>]. In this study, the absence of an effect of HIV infection on relapse rates after receipt of a 6-month regimen of rifampin—at odds with our overall findings (<xref rid="fig1" ref-type="fig">figure 1</xref>)—may also relate to the unusually high competitive risk of reinfection. In any case, the equal or higher proportion of reinfections among the higher number of recurrences among HIV-infected patients and the sensitivity of overall recurrence rates to treatment duration suggest that HIV infection increases risks for both relapse and reinfection.</p>
<p>In countries where HIV infection is highly endemic, many patients who have TB receive only 2 months of rifampin treatment. For example, of 10 sub-Saharan African countries that have a high TB burden and that use DOTS, 7 use regimens with just 2 months of rifampin therapy, and 3 use regimens with 6 months of rifampin therapy throughout. Our results underline the importance of the 6-month minimum duration, especially in countries where HIV infection is endemic. HIV-infected patients might benefit from further prolongation of treatment beyond 6 months (<xref rid="fig1" ref-type="fig">figure 1</xref>) or receipt of preventive treatment with isoniazid, although such protection from recurrent TB may confer only a small increase in survival [<xref rid="ref8" ref-type="bibr">8</xref>, <xref rid="ref35" ref-type="bibr">35</xref>]. Improved outcome of TB treatment would decrease the TB case load for health facilities (depending on the proportion of re-treatments) and might reduce TB transmission in the community. These possible benefits will have to be weighed against treatment side effects, feasibility (including the risks of noncompliance and development of drug resistance), and the financial and human resources needed for prolonged treatment versus re-treatment.</p>
<p>In conclusion, the increased rate of recurrence of TB among HIV-infected patients probably reflects both increased rates of reinfection and increased rates of relapse. The recurrence risk is especially elevated with treatment regimens involving <6 months of rifampin, underscoring the importance for countries where HIV infection is endemic to promote use of regimens that include 6 months of rifampin therapy administered under DOTS policy.</p>
</sec>
</body>
<back>
<ack>
<title>Acknowledgments</title>
<p>We thank Eleanor Gouws, for statistical advice, Pamela Baillie, for assistance in literature search, and Elizabeth Corbett, Peter Godfrey-Faussett, Anthony Harries, and Rick O'Brien, for comments on the design of the study and the manuscript.</p>
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<fpage>550</fpage>
<lpage>2</lpage>
</nlm-citation>
</ref>
</ref-list>
<sec sec-type="display-objects">
<title>Figures and Tables</title>
<fig position="anchor" id="fig1">
<label>Figure 1</label>
<caption>
<p>Figure 1. Tuberculosis (TB) recurrence rates for patients stratified by HIV infection status and duration of rifampin (Rif) therapy, as estimated by multivariate regression. The significance of the differences was as follows: HIV infection status, <italic>P</italic> <.0001; Rif therapy for 2–3 months (mo) versus 5–6 mo, <italic>P</italic> =.0002; Rif therapy for 2–3 mo versus ⩾7 mo, <italic>P</italic> <.0001; Rif therapy for 5–6 mo versus ⩾7 mo, <italic>P</italic> =.17; and interaction between HIV infection status and duration of Rif therapy, <italic>P</italic> =.025. Prediction for covariate levels: follow-up duration, 34.1 mo; TB incidence, 250 cases per 100,000 person-years. Error bars represent 95% CIs. +, Positive, -, negative.</p>
</caption>
<graphic mimetype="image" xlink:href="37-1-101-fig001.tif"></graphic>
</fig>
<fig position="anchor" id="fig2">
<label>Figure 2</label>
<caption>
<p>Figure 2. Tuberculosis (TB) recurrence rates (per 100 person-years) over time for HIV-uninfected patients <italic>(top)</italic> and HIV-infected patients <italic>(bottom)</italic> after rifampin therapy. Each point represents the mean time of the follow-up interval to which the observed recurrence rate refers. Most studies are represented by multiple points, one for each time interval for which they specified a recurrence rate or number. Error bars indicate the 95% CIs for the data points. For HIV-uninfected patients, the Weibull curve best describing the data has the following coefficients (corresponding to rates per 100 person-years): α = 0.0324 ± 0.0144 and β = 0.422 ± 0.027. For HIV-infected patients, the shape coefficient <italic>β</italic> does not differ significantly from 1 (exponential survivorship, constant hazard), so we set β = 1, and the best-fitting value of <italic>α</italic> is then 6.71 × 10<sup>-3</sup> ± 0.876 × 10<sup>-3</sup>. In the top panel, the upper left data point for which the 95% CI falls out of the fitted curve is from 1 of the 3 studies that used only 2 months of rifampin therapy [<xref rid="ref21" ref-type="bibr">21</xref>].</p>
</caption>
<graphic mimetype="image" xlink:href="37-1-101-fig002.tif"></graphic>
</fig>
<fig position="anchor" id="tab1">
<label>Table 1</label>
<caption>
<p>Table 1. Key outcomes of included studies of the recurrence of tuberculosis (TB) after receipt of rifampin-based treatment, by HIV infection status.</p>
</caption>
<graphic mimetype="image" xlink:href="37-1-101-tbl001.tif"></graphic>
</fig>
<fig position="anchor" id="tab2">
<label>Table 2</label>
<caption>
<p>Table 2. Summary outcomes of reviewed studies on the rate and cause of tuberculosis (TB) recurrence, by HIV infection status, and crude risk ratios, weighted by study size.</p>
</caption>
<graphic mimetype="image" xlink:href="37-1-101-tbl002.tif"></graphic>
</fig>
</sec>
</back>
</article></istex:document></istex:metadataXml><mods version="3.6"><titleInfo><title>Effects of Human Immunodeficiency Virus Infection on Recurrence of Tuberculosis after Rifampin-Based Treatment: An Analytical Review</title></titleInfo><titleInfo type="alternative" contentType="CDATA"><title>Effects of Human Immunodeficiency Virus Infection on Recurrence of Tuberculosis after Rifampin-Based Treatment: An Analytical Review</title></titleInfo><name type="personal"><namePart type="given">Eline L.</namePart><namePart type="family">Korenromp</namePart><affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Fabio</namePart><namePart type="family">Scano</namePart><affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</affiliation><affiliation>E-mail: scanof@who.int</affiliation><affiliation>Dr. Fabio Scano, World Health Organization, Communicable Diseases, StopTB Dept., Avenue Appia 20, CH 1211, Geneva 27, Switzerland</affiliation><affiliation>E-mail: scanof@who.int</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Brian G.</namePart><namePart type="family">Williams</namePart><affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Christopher</namePart><namePart type="family">Dye</namePart><affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Paul</namePart><namePart type="family">Nunn</namePart><affiliation>Communicable Diseases, Stop TB Department, World Health Organization, Geneva, Switzerland</affiliation><role><roleTerm type="text">author</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="research-article" displayLabel="research-article" authority="ISTEX" authorityURI="https://content-type.data.istex.fr" valueURI="https://content-type.data.istex.fr/ark:/67375/XTP-1JC4F85T-7">research-article</genre><originInfo><publisher>The University of Chicago Press</publisher><dateIssued encoding="w3cdtf">2003-07-01</dateIssued><copyrightDate encoding="w3cdtf">2003</copyrightDate></originInfo><abstract>We reviewed 47 prospective studies of recurrence of pulmonary tuberculosis (TB) after cure to assess the influence of human immunodeficiency virus (HIV) infection and rifampin treatment. Multivariate regression revealed that the recurrence rate for HIV-uninfected persons increased with decreasing duration of therapy: it was 1.4 cases per 100 person-years for recipients of ⩾7 months of rifampin therapy and 2.0 and 4.0 cases per 100 person-years for recipients of 5–6 and 2–3 months of rifampin therapy, respectively (trend P =.00014), over a mean follow-up duration of 34 months, at a TB incidence of 250 cases per 100,000 person-years. Relative risks of recurrence associated with HIV infection at these 3 treatment durations were 2.2, 2.1, and 3.4, respectively, with a significant interaction between HIV infection status and treatment duration (P =.025). The recurrence rate increased with the background TB incidence (P =.048), and it decreased over time since completion of treatment in HIV-uninfected but not in HIV-infected patients (overall trend, P =.00008; difference by HIV infection status, P =.025). In countries where HIV infection is endemic, TB recurrence may be reduced by administration of rifampin-based treatment for at least 6 months, in accordance with World Health Organization recommendations.</abstract><relatedItem type="host"><titleInfo><title>Clinical Infectious Diseases</title></titleInfo><titleInfo type="abbreviated"><title>Clinical Infectious Diseases</title></titleInfo><genre type="journal" authority="ISTEX" authorityURI="https://publication-type.data.istex.fr" valueURI="https://publication-type.data.istex.fr/ark:/67375/JMC-0GLKJH51-B">journal</genre><identifier type="ISSN">1058-4838</identifier><identifier type="eISSN">1537-6591</identifier><identifier type="PublisherID">cid</identifier><identifier type="PublisherID-hwp">cid</identifier><part><date>2003</date><detail type="volume"><caption>vol.</caption><number>37</number></detail><detail type="issue"><caption>no.</caption><number>1</number></detail><extent unit="pages"><start>101</start><end>112</end></extent></part></relatedItem><identifier type="istex">280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D</identifier><identifier type="DOI">10.1086/375220</identifier><accessCondition type="use and reproduction" contentType="copyright">© 2003 by the Infectious Diseases Society of America</accessCondition><recordInfo><recordContentSource authority="ISTEX" authorityURI="https://loaded-corpus.data.istex.fr" valueURI="https://loaded-corpus.data.istex.fr/ark:/67375/XBH-GTWS0RDP-M">oup</recordContentSource><recordOrigin>© 2003 by the Infectious Diseases Society of America</recordOrigin></recordInfo></mods><json:item><extension>json</extension><original>false</original><mimetype>application/json</mimetype><uri>https://api.istex.fr/document/280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D/metadata/json</uri></json:item></metadata><covers><json:item><extension>tiff</extension><original>true</original><mimetype>image/tiff</mimetype><uri>https://api.istex.fr/document/280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D/covers/tiff</uri></json:item><json:item><extension>html</extension><original>true</original><mimetype>text/html</mimetype><uri>https://api.istex.fr/document/280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D/covers/html</uri></json:item></covers><annexes><json:item><extension>jpeg</extension><original>true</original><mimetype>image/jpeg</mimetype><uri>https://api.istex.fr/document/280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D/annexes/jpeg</uri></json:item><json:item><extension>gif</extension><original>true</original><mimetype>image/gif</mimetype><uri>https://api.istex.fr/document/280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D/annexes/gif</uri></json:item><json:item><extension>pdf</extension><original>true</original><mimetype>application/pdf</mimetype><uri>https://api.istex.fr/document/280FCACCA126DE4F5F8B2EDA0D31A2B049AB8A2D/annexes/pdf</uri></json:item></annexes><serie></serie></istex></record>Pour manipuler ce document sous Unix (Dilib)
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