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Trends in overall opportunistic illnesses, Pneumocystis carinii pneumonia, cerebral toxoplasmosis and Mycobacterium avium complex incidence rates over the 30 years of the HIV epidemic: a systematic review.

Introduction

The natural history of human immunodeficiency virus (HIV) infection and acquired immunodeficiency syndrome (AIDS) has changed dramatically since the onset of the epidemic in the 1980s. The landmark of this process was the introduction of highly active antiretroviral therapy (ART) in 1996. Despite the progress made in the treatment and control of HIV infection, HIV/AIDS persists as one of the main causes of death in the world, affecting individuals from both high-income and low-income settings. (1) In addition, although an increase in non-AIDS associated morbidity and mortality has been observed, opportunistic infections remain a major cause of hospitalization and death in people living with HIV/AIDS in high and low-income settings. (2-4)

Currently, in the post-ART period, opportunistic illnesses are mainly related with late diagnosis and/or presentation to care, non-adherence to ART and HIV resistance to antiretroviral drugs. (2,5) Late diagnosis and/or presentation to care is one of the most challenging aspects of the HIV epidemic. In Brazil, 34% of the patients still present with an opportunistic illness at the moment of ART initiation. (6) Furthermore, non-adherence to ART results in virologic failure and disease progression. Factors associated with non-adherence, such as low educational level, young age, unemployment, alcoholism and use of illicit drugs represent an important socioeconomic problem, in particular for low/middle-income settings. (7,8) Finally, multidrug resistance to antiretroviral drugs is a consequence of HIV exposure to ART, particularly in settings where non-adherence prevails. (9)

In this study, we review the trends in opportunistic illnesses incidence rates and compare the results observed in high-income settings (HIS) with that for low/middle-income settings (LMIS), with special attention given to studies from Brazil. We evaluate the impact ART has had in three specific opportunistic infections of particular importance to Brazil and contrast the patterns in the countries evaluated.

Search strategy and selection criteria

Publications related to AIDS-associated opportunistic illnesses incidence were identified by systematically searching in Pubmed, Web of Science, Lilacs and Google scholar. Publications were restricted to the following languages: English, Portuguese, and Spanish. The databases were searched for studies published until January 2013 using the following search terms and Boolean operators, for matches under any field: (incidence) AND (HIV OR human immunodeficiency virus) AND (AIDS-defining illness OR opportunistic infection OR opportunistic disease OR AIDS-related opportunistic infection OR AIDS-related opportunistic illness). For the Lilacs database, search terms were translated into Portuguese language and separate searches with each term were conducted. Titles and available abstracts were scanned for relevance identifying papers requiring further consideration. Bibliographies of relevant articles were also checked. Inclusion criteria consisted in (1) presence of a person-time denominator and (2) results for all opportunistic illnesses and/or the three opportunistic infections of interest, namely: Pneumocystis carinii pneumonia (PCP), cerebral toxoplasmosis (NTX) and Mycobacterium avium complex (MAC). Exclusion criteria included: (1) results given only for hospitalization and/or severe diseases, (2) results given relative terms only (that is, as incidence rate ratios, odds ratios or relative risks), (3) results given only for Immune Reconstitution Inflammatory Syndrome, and (4) results that aggregate death and opportunistic infections in one outcome. The results, inclusion and exclusion criteria are shown in Fig. 1.

Results

Thirty seven publications met the study's eligibility criteria, 25 from HIS and 12 studies from LMIS (Fig. 1). (2,10-45) Out of the 12 studies from LMIS, four were from Latin America, specifically from Brazil. Results from these studies are summarized in the next sections with incidence rates in 100 person-years (100 PY) format.

Opportunistic illnesses

Table 1 summarizes the findings for the incidence rate of opportunistic illnesses from 1984 to 2010 in HIS and LMIS. Depending on the study, incidence rates ranged from 2.3 to 12.3 times lower in the post-ART period compared to the pre-ART period.

In HIS, a multicenter study conducted in the United States using data from the HIV Outpatient Study (HOPS) cohort with no CD4+ cell count restriction of the study population reported that the incidence rate of opportunistic illnesses decreased from 9.24/100 PY in pre-ART period to 1.66/100 PY in post-ART period. (2) A more striking result was reported for the Eurosida cohort, an European multicenter cohort that included only patients with CD4+ cell counts less than 500 cells/[mm.sup.3] where the incidence rate of opportunistic illnesses decreased from 30.7/100 PY in the pre-ART period to 2.5/100 PY in the post-ART period. (10) Similarly, a study from Spain that included patients with CD4+ cell counts less than 500 cells/mm3 reported significant decreases in the incidence rate of opportunistic illnesses, which went from 43.2/100 PY to 14.6/100 PY, in the pre and post-ART periods, respectively. (11) Other studies conducted in HIS can be found in Table 1, including results from England, Canada, Switzerland and Germany.

In LMIS, in a study from Thailand with no CD4+ cell count restriction of the study population, the incidence rate of opportunistic illnesses decreased from 19.1/100 PY in the absence of ART to 8.2/100 PY after ART use. (12) A study conducted in Sao Paulo in the period of 1986 through 1997, also with no CD4+ cell count restriction of the study population, reported an incidence rate of opportunistic illnesses of 12.24/100 PY in a supposedly pre-ART period. (13) Another study conducted with the same population during the period from 1987 to 2002 estimated a lower incidence rate of opportunistic illnesses of 4.6/100 PY. (14) A study from Rio de Janeiro, that included only patients with CD4+ counts less than 100 cells/ (mm) 3 in the period of 1997 to 1999, found an incidence rate of opportunistic illnesses of 29/100 PY a supposedly post-ART period. (15) Other

studies conducted in LMIS can be found in Table 1 and include results from South Africa, Ivory Coast, Senegal and Poland.

Pneumocystis carinii pneumonia

Table 2 summarizes the findings for PCP incidence rates from 1982 to 2008 in HIS and LMIS. Depending on the study, incidence rates ranged from 2.0 to 15.6 times lower in the post-ART period compared to the pre-ART period.

In HIS, a study conducted in one center in England including all HIV-infected individuals showed that the incidence rate of PCP decreased from 9.1/100 PY in the pre-ART period (before 1992) to 1.9/100 PY in the post-ART period (in 1997). (16) An even more dramatic result was reported in a study from San Francisco, United States, that used local surveillance data of the HIV-infected population and showed that the incidence rate of PCP dropped from 9.5/100 PY in pre-ART period (1993-1995) to 0.85/100 PY in post-ART period (2001-2008). (17) Other studies conducted in HIS can be found in Table 2, including results from France, Spain, Switzerland and Germany.

In LMIS, a study from Taiwan that included all HIV-infected individuals estimated that the incidence rate of PCP decreased from 70.5/100 PY in the pre-ART period (1995) to 9.2/100 PY in the post-ART period (1999). (18) In addition, a study from Thailand that, again, included all HIV-infected patients reported an incidence rate of PCP decreasing from 4.7/100 PY in the absence of ART to 0.3/100 PY after ART use. (12) Other studies conducted in LMIS can be found in Table 2 and include results from South Africa and Poland. Unfortunately, we found no study from Brazil.

Cerebral toxoplasmosis

Table 3 summarizes the findings for NXT incidence rate from 1985 to 2010 in HIS and LMIS. Depending on the study, incidence rates varied from 1.2 to 8.0 times lower in the post-ART period compared to the pre-ART period.

In HIS, a multicenter cohort (Multicenter AIDS Cohort Study--MACS) of HIV-infected men who have sex with men from the United States reported that the incidence rate of NTX decreased from 0.54/100 PY in pre-ART period (1990-1992) to 0.22/100 PY in post-ART period (1996-1998).19 Data of the Swiss cohort (multicenter cohort) confirmed this trend showing that the incidence rate of NTX among HIV-infected individuals who started antiretroviral therapy between 1995 and 1997 decreased from 1.45/100 PY before ART use to 0.18/100 PY after ART use. (20) Also in HIS, in a multicenter study from United Kingdom conducted among HIV-infected individuals reported that the incidence rate of NTX decreased from 0.32/100 PY in the pre-ART period (1996-1997) to 0.04/100 PY in the post-ART period (1996-2007). (21) Other studies conducted in HIS can be found in Table 3, including results from England, France, Spain, Switzerland and Germany.

In LMIS, a study from Thailand that included all HIV-infected patients estimated a reduction in the incidence rate of NTX from 1.2/100 PY in the absence of ART to 1.0/100 PY after ART use. (12) Data from LMIS also include a study from South Africa, with no [CD4.sup.+] cell count restriction of the study population, with an incidence rate of NTX of 0.15/100 PY in the period of 1992-2000. (22) Again, we unfortunately did not find any study from Brazil.

Mycobacterium avium complex disease

Table 4 summarizes the findings for MAC incidence rate from 1985 to 2008 in HIS and LMIS. Depending on the study, incidence rates ranged from 2.4 to 25.8 times lower in the post-ART period compared to the pre-ART period.

In HIS, a surveillance study from San Francisco (United States), with no [CD4.sup.+] cell count restriction of the study population, reported an incidence rate of MAC decreasing from 8.52/100 PY in pre-ART period (1993-1995) to 0.32/100 PY in post-ART period (2001-2008). (17) One study from Spain, that included only patients with CD4+ counts less than 500 cells/[mm.sup.3], reported that the incidence rate of MAC decreased from 2.9/100 PY in pre-ART period (1992) to 0.6/100 PY in post-ART period (1997). (11) In addition, data from the Swiss Cohort for patients with [CD4.sup.+] counts less than 50 cells/[mm.sup.3], showed an incidence rate of MAC decreasing from 8.8/100 PY in pre-ART period (1990-1996) to 1.4/100 PY in post-ART period (1997-1999). (23) Other studies conducted in HIS can be found in Table 4, including results from England, France, Spain, Switzerland, and Germany.

In LMIS, two studies from Africa and one from Brazil report incidence rates of MAC. The South African study, with no [CD4.sup.+] cell count restriction of the study population reported an incidence rate of 0.4/100 PY for the period of 1992-2000. (22) Another study, from Ivory Coast including all HIV-infected found an incidence rate of 1.85/100 PY for the period of 1992-2002. (24) The study from Brazil, conducted from 1997 to 1999 among patients with CD4+ cell counts less than 100 cells/[mm.sup.3] reported no cases of disseminated MAC. (25)

Discussion

Through a systematic review of the literature, we have shown that the incidence of opportunistic illnesses decreased over the 30 years of the HIV epidemic, markedly after ART availability. The significant reduction in the incidence rates was demonstrated for opportunistic illnesses overall and also for specific opportunistic infections, namely, PCP, NXT and MAC. In addition, the decreasing trends were shown for both HIS and LMIS where ART was made available. This result is extremely positive as it shows that opportunistic illnesses can be controlled while also pointing to the persistent challenge of a timely diagnosis of HIV infection. Indeed, in order to control opportunistic illnesses HIV infection status must be identified and earlier linkage to care needs to be facilitated. That is, a higher uptake of HIV testing with direct linkage to care of those found to be HIV-infected is urgently needed.

We found that the magnitude of the incidence rates and of the reduction of these rates as a function of ART varied between studies. Indeed, it is well known that there are geographical differences in the incidence of opportunistic illnesses. (26) Other reasons for the differences in the baseline rates might include different study populations, including different sociodemographic subgroups evaluated in a specific study, for example, the MACS cohort that focuses on men who have sex men, (27) as well as different inclusion criteria. Some studies included all HIV-infected individuals while others restricted the study population to individuals with specific CD4+ cell counts, for example, including only those with CD4+ cell count less than 100 cells/[mm.sup.3]. (15) Moreover, different study definitions with respect to the diseases chosen to be included in any given study might have further contributed to the disparate results.

Out of the 37 studies included in the present review, almost 70% were from HIS. Of the 12 studies from LMIS, four studies were from Brazil. (13-15,25) These studies reported incidence rates for opportunistic illnesses for the entire study period included in the respective study and not annual rates that could allow us to evaluate the temporal trends in incidence. Also, only one study from Brazil reported separately on the incidence rate of MAC. However, this study reported no cases of the disease, a finding that could have been due to the small sample size and/or short follow-up. For other important diseases that define the AIDS epidemic, namely, PCP, and NXT, no studies from Brazil were found. Furthermore, all are single center cohort studies, two from Sao Paulo (Hospital das Clinicas, Faculdade de Medicina da Universidade de Sao Paulo) and two from Rio de Janeiro (Instituto de Pesquisa Clinica Evandro Chagas, Fundacao Oswaldo Cruz). We believe that the description of the trends in incidence rates of opportunistic illnesses is of paramount value to health care providers to guide clinical decision-making and policy makers to define priorities for care and prevention of opportunistic infections.

Strengths and limitations to the present study are worth mentioning. Through a systematic review conducted in four databases we found the epidemiological studies that reported on the incidence rate of opportunistic illnesses. We restricted the review to those studies reporting on rates (and not overall numbers or frequencies) since this epidemiological parameter is adjusted for population size and time under risk thus allowing for comparisons between studies. Though not a limitation of our study design and approach, the scarcity of studies from LMIS implies that we cannot adequately describe the patterns of incidence in these settings. In addition, the few studies found should also not be understood as representative of entire countries as they report from one center only. Finally, the different study methodologies such as inclusion criteria and diseases included, for example, limited the comparisons.

In conclusion, the incidence rate of opportunistic illnesses has decreased over time mainly due to the availability of highly effective, safe and well tolerated ART. However, a public health challenge remains for future years. Public health policies focusing on earlier HIV diagnosis and linkage to care, adherence and retention programs, and surveillance of HIV multidrug resistance in populations should be developed and implemented with the goal of improving the quality of life and reducing morbidity and mortality among HIV-infected individuals. To better understand the nuances of the epidemiology of opportunistic illnesses in LMIS, multicenter cohort studies should be encouraged. Finally, it is clear that studies from Brazil are urgently needed to assess the current burden of opportunistic illnesses in order to support the planning of HIV/AIDS health care services organization.

Sources of funding

BG acknowledges funding from the National Council of Technological and Scientific Development (CNPq) and the Research Funding Agency of the State of Rio de Janeiro (FAPERJ). PML acknowledges funding from the National Council of Technological and Scientific Development (CNPq).

Conflicts of interest

The authors declare no conflicts of interest.

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ARTICLE INFO

Article history:

Received 5 August 2013

Accepted 12 October 2013

Available online 23 November 2013

Lara Coelho *, Valdilea Goncalves Veloso, Beatriz Grinsztejn, Paula Mendes Luz

Instituto de Pesquisa Clinica Evandro Chagas, Fundacao Oswaldo Cruz, Rio de Janeiro, Brazil

* Corresponding author at: Instituto de Pesquisa Clinica Evandro Chagas, Fundacao Oswaldo Cruz, Avenida Brasil 4365, Manguinhos, Rio de Janeiro, CEP 21045-900, Rio de Janeiro, Brazil.

E-mail addresses: lara.coelho@ipec.fiocruz.br, laraesteves@gmail.com (L. Coelho).

http://dx.doi.org/10.1016/j.bjid.2013.10.003

Table 1--Incidence rates for opportunistic illnesses among
HIV-infected individuals from high and low/middle-income settings.

First author, year,          Setting and cohort      Time period
journal                       (when applicable)        evaluated

High-income settings
  Cain, 2009, American       Baltimore,            1984a to April
    Journal of               Pittsburgh, Chicago   2007
    Epidemiology             and Los Angeles,
                             US, MACS cohort

  Mocroft, 1999, Journal     London, UK, Royal     1987 (a) to
    of Acquired Immune       Free Center for HIV   1998 (a)
    Deficiency Syndromes     Medicine

  San-Andres, 2003,          Madrid, Spain,        January 1989-
    Clinical Infectious      University Hospital   1997 (a)
    Diseases

  Charurat, 2004, Journal    4 states in US and    December 1989 to
    of Women's Health        Puerto Rico, WITS     June 2002
                             Cohort

  Kaplan, 2000, Clinical     10 US cities,         1992 (a) to
    Infectious Diseases      Adults/Adolescents    September 1999
                             Spectrum of HIV
                             Disease (ASD) Study

  Forrest, 1998, Clinical    British Columbia,     January 1994 to
    Infectious Diseases      Canada, British       December 1996
                             Columbia Center for
                             Excellence in
                             HIV/AIDS

  Mocroft, 2000, Lancet      51 centers in         May 1994 to
                             Europe, Eurosida      spring 1999 (a)
                             cohort

  Buchacz, 2010, AIDS        12 centers in US,     January 1994 to
                             HOPS cohort           December 2007

  Ledergerber, 1999,         7 centers in          September 1995 to
    Journal of the           Switzerland, Swiss    March 1999
    American Medical         HIV Cohort Study
    Association

  Wohl, 2003, Aids Patient   10 US cities, ASD     1996 (a( to
    Care and STDs            cohort                2000 (a)

  Plettenberg, 2011,         Germany, KompNet      1996 (a) to
    Infection                cohort                2010 (f)

Low/middle-income settings
  Fonseca, 1999,             Sao Paulo, Brazil,    1986 (a) to
    International Journal    University of Sao     June 1997
    of Epidemiology          Paulo

  Casseb, 2003, AIDS         Sao Paulo, Brazil,    October 1987 to
    Patient care and STDs    University of Sao     February 2002
                             Paulo

  Badri, 2005, The           Cape Town, South      1992 (a) to
    Southern African         Africa, Cape Town     December 2000
    Journal of HIV           AIDS Cohort (CTAC)
    Medicine

  Losina, 2007, Antiviral    Abidjan, Ivory        1996 (a) to
    Therapy                  Coast, Cotrimo CI     July 2003
                             ANRS 059 and
                             Cotrame ANRS1203

  Gadelha, 2002, Rev Inst    Rio de Janeiro,       September 1997 to
    Med Trop Sao Paulo       Brazil, IPEC cohort   December 1999

  De Beaudrap, 2010, BMC     Senegal, Initative    August 1998 to
    Infectious Diseases      Senegalaise d'Acess   April 2008
                             aux medicaments
                             Antiretroviraux (k)

  Podlasin, 2006,            10 centers in         2000 (a) to
    Infection                Poland                2002 (a)

  Rojanawiwat, 2011,         Lampang, Thailand,    July 2000 to
    International Health     Governmental          October 2004
                             Referral
                             Hospital (1)

First author, year,            Incidence rate estimate
journal

High-income settings
  Cain, 2009, American       Entire period: 5.23/100 PY;
    Journal of               Before 1996: 7.53/100 PY;
    Epidemiology             After1996: 2.19/100 PY

  Mocroft, 1999, Journal     Before 1992: 27.4/100 PY;
    of Acquired Immune       1992-1993: 16.8/100 PY;
    Deficiency Syndromes     1994: 17.9/100 PY; 1995:
                             19.3/100 PY; 1996: 16.7/100
                             PY; 1997: 6.9/100 PY

  San-Andres, 2003,          1989-1991: 36.4/100 PY;
    Clinical Infectious      1992: 43.2/100 PY; 1993:
    Diseases                 39.0/100 PY; 1994: 32.4/100
                             PY; 1995: 32.0/100 PY; 1996:
                             30.9/100 PY; 1997: 14.6/100
                             PY

  Charurat, 2004, Journal    Before Feb/1994: 4.52/100
    of Women's Health        PY; Mar/1994 to Jul/1996:
                             5.09/100 PY; After Aug/1996:
                             1.22/100 PY

  Kaplan, 2000, Clinical     1996-1998: 16/100 PY (c)
    Infectious Diseases

  Forrest, 1998, Clinical    1994: 8/100 PY; 1996: 2.2/100
    Infectious Diseases      PY

  Mocroft, 2000, Lancet      1994: 30.7/100 PY; 1998:
                             2.5/100 P (c)

  Buchacz, 2010, AIDS        1994-1997: 9.24/100 PY;
                             1998-2002: 2.96/100 PY;
                             2003-2007: 1.66/100 PY

  Ledergerber, 1999,         Before to ART use: 15.1/100
    Journal of the           PY; after ART use: 3.57/100
    American Medical         PY
    Association

  Wohl, 2003, Aids Patient   US born: 21.0/100 PY;
    Care and STDs            Mexican born: 16.6/100 PY;
                             Central American born:
                             13.9/100 PY

  Plettenberg, 2011,         Group 1: 1.38/100 PY; Group
    Infection                2: 0.78/100 PY

Low/middle-income settings
  Fonseca, 1999,             12.24/100 PY (converted
    International Journal    from 10.2/1000 PM)
    of Epidemiology

  Casseb, 2003, AIDS         4.6/100 PY (converted from
    Patient care and STDs    3.84/1000PM)

  Badri, 2005, The           21.34/100 PY
    Southern African
    Journal of HIV
    Medicine

  Losina, 2007, Antiviral    Cotrimoxazole alone: CD4
    Therapy                  less than 50 cells/[mm.sup.3]:
                             20.17/100 PY; CD4 above 200
                             cells/[mm.sup.3]: 3.54/100 PY;
                             Cotrimoxazole plus ART
                             (0-6 months): CD4 less 50
                             cells/[mm.sup.3]: 20.22/100 PY,
                             CD4 > 200 cells/[mm.sup.3]:
                             2.79/100 PY; Cotrimoxazole
                             plus ART (>6 months):
                             CD4 < 50 cells/[mm.sup.3]:
                             6.84/100 PY, CD4 > 200
                             cells/[mm.sup.3]: 1.68/100 PY

  Gadelha, 2002, Rev Inst    29/100 PY (j)
    Med Trop Sao Paulo

  De Beaudrap, 2010, BMC     First year after ART
    Infectious Diseases      initiation: 20.5/100 PY. Over
                             the fourth year after ART
                             initiation: 4.3/100 PY

  Podlasin, 2006,            Total: 2.4/100 PY; 2000:
    Infection                6.8/100 PY; 2001: 6.5/100 PY;
                             2002: 4.8/100 PY

  Rojanawiwat, 2011,         Prior to ART: 19.1/100 PY;
    International Health     After ART use: 8.2/100 PY

First author, year,                     Notes
journal

High-income settings
  Cain, 2009, American       Patient inclusion criteria: no CD4
    Journal of               criteria, MSM only; Disease definition:
    Epidemiology             CDC 1993, considers only the first ADI
                             after cohort enrollment

  Mocroft, 1999, Journal     Patient inclusion criteria: no CD4
    of Acquired Immune       criteria; Disease definition: CDC 1993,
    Deficiency Syndromes     considers only the first ADI after
                             cohort enrollment

  San-Andres, 2003,          Patient inclusion criteria: CD4 less
    Clinical Infectious      than 500 cells/[mm.sup.3] or previous
    Diseases                 AIDS diagnosis; Disease definition: not
                             clearly  stated, likely considers all
                             ADI (b) episodes after cohort
                             enrollment

  Charurat, 2004, Journal    Patient inclusion criteria: no CD4
    of Women's Health        criteria, only women without previous
                             diagnosis of AIDS; Disease definition:
                             CDC 1993; considers only the first ADI
                             after cohort enrollment

  Kaplan, 2000, Clinical     Patient inclusion criteria: no CD4
    Infectious Diseases      criteria; Disease definition: not
                             clearly stated, likely considers all ADI
                             (d) episodes after cohort enrollment

  Forrest, 1998, Clinical    Patient inclusion criteria: no CD4
    Infectious Diseases      criteria, included only patients in use
                             of antiretroviral drugs; Disease
                             definition: CDC 1993; considers only the
                             first ADI after cohort enrollment

  Mocroft, 2000, Lancet      Patient inclusion criteria: CD4 < 500
                             cells/[mm.sup.3]; Disease definition:
                             CDC 1993, considers the first ADI after
                             cohort enrollment

  Buchacz, 2010, AIDS        Patient inclusion criteria: no CD4
                             criteria; Disease definition: CDC 1993
                             (e); considers only the first ADI after
                             cohort enrollment

  Ledergerber, 1999,         Patient inclusion criteria: no CD4
    Journal of the           criteria, included patients who started
    American Medical         ART between September 1995 and December
    Association              1997. Disease definition: CDC 1993,
                             considers only the first ADI after
                             cohort enrollment

  Wohl, 2003, Aids Patient   Patient inclusion criteria: no CD4
    Care and STDs            criteria; included US born Latinos,
                             Mexican born Latinos and Central
                             American Latinos. Disease definition:
                             not clear stated, apparently included
                             all ADI presented in the study period.

  Plettenberg, 2011,         Patient inclusion criteria: patients who
    Infection                started antiretroviral treatment. (g)
                             Disease definition: included the first
                             episode of an ADI after antiretroviral
                             therapy.

Low/middle-income settings
  Fonseca, 1999,             Patient inclusion criteria: asymptomatic
    International Journal    patients; Disease definition: CDC 1987,
    of Epidemiology          modified to include pulmonary
                             tuberculosis as an AIDS defining-
                             condition, considers only the first ADI
                             after cohort enrollment

  Casseb, 2003, AIDS         Patient inclusion criteria: asymptomatic
    Patient care and STDs    patients; Disease definition: CDC 1987,
                             considers only the first ADI after
                             cohort enrollment

  Badri, 2005, The           Patient inclusion criteria: no CD4
    Southern African         criteria; Disease definition: WHO 1990,
    Journal of HIV           considers all ADI episodes after cohort
    Medicine                 enrollment

  Losina, 2007, Antiviral    Patient inclusion: Patients
    Therapy                  participating in Cotrimo ANRS and
                             Cotrame ANRS studies. Disease
                             definition: considers only the first ADI
                             (h) presented in each period (i) of
                             study. Results were stratified by use of
                             cotrimoxazole prophylaxis, ART and CD4
                             counts.

  Gadelha, 2002, Rev Inst    Patient inclusion criteria: at least one
    Med Trop Sao Paulo       CD4 < 100 cells/[mm.sup.3], included
                             patients who started ART between
                             September 1995 and December 1997.
                             Disease definition: CDC 1993, considers
                             the first ADI after cohort enrollment

  De Beaudrap, 2010, BMC     Patient inclusion criteria: no CD4
    Infectious Diseases      criteria. Disease definition: CDC 1993,
                             considered the first episode of each ADI
                             presented after ART initiation. Results
                             were stratified by timing of ART use

  Podlasin, 2006,            Patient inclusion criteria: none;
    Infection                Disease definition: CDC 1993, not
                             clearly stated, likely considers all ADI
                             after cohort enrollment

  Rojanawiwat, 2011,         Patient inclusion criteria: no CD4
    International Health     criteria; Disease definition: included
                             the first episode of all ADI (m)
                             presented by the patient

ADI: AIDS defining illness; CDC: Centers for Disease Control; CMV:
cytomegalovirus; MAC: Mycobacterium avium complex; MSM: men who
have sex with men; PCP: Pneumocystis carinii pneumonia.

(a) Month not specified.

(b) Does not specify the criteria used for ADI, the results
include: Esophageal candidiasis, PCP, tuberculosis, wasting syndrome,
cerebral toxoplasmosis, Kaposi's sarcoma, AIDS dementia complex,
progressive multifocal leukoencephalopathy, primary brain lymphoma,
CMV disease, MAC, non-Hodgkin lymphoma, cryptosporidiosis, recurrent
pneumonia, cryptococcosis, chronic herpes simplex, invasive cervical
cancer.

(c) Results for other years shown in figure format only, thus not
reported here.

(d) Diseases included: PCP, disseminated MAC, cerebral
toxoplasmosis, Kaposi's sarcoma, CMV retinitis, esophageal
candidiasis, cryptococcosis.

(e) Excluded diseases: recurrent pneumonia, Salmonella septicemia
and wasting syndrome.

(f) Time inferred from information contained in the text.

(g) Patients were separated into two groups: Group 1: patients who
started ART with CD4 between 250 and 349 cells/[mm.sup.3]; Group 2:
patients who started ART with CD4 between 350 and 450 cells/
[mm.sup.3].

(h) Diseases included: severe bacterial infections (pneumonia,
enteritis, bacteremia, invasive urogenital infection), malaria,
cerebral toxoplasmosis, isosporosis, PCP, extrapulmonar
cryptococosis, esophageal candidiasis, tuberculosis, MAC, other
WHO clinical stage 3 and 4.

(i) In the first period (until December 1998), patients received
cotrimoxazole prophylaxis. In the second period (after December
1998) patients received ART plus cotrimoxazole prophylaxis (the
later period was separated in the first 6 months after ART
initiation and after 6 months of ART initiation).

(j) Data from de prospective period.

(k) Antiretroviral drugs available for free since December 2003.

(l) In 2002 the government introduced the co-formulation stavudine,
lamivudine and nevirapine (on a pilot basis). The use of this
medication gradually increased especially after 2004.

(m) Does not specify the criteria used for ADI, the results include:
tuberculosis, PCP, cryptococcal meningitis, penicilliosis,
esophageal candidiasis, herpes zoster, cerebral toxoplasmosis, CMV
retinitis.

Table 2--Incidence rate for Pneumocystis carinii pneumonia among
HIV-infected individuals from high and low/middle-income settings.

First author, year, journal   Setting and cohort      Time period
                               (when applicable)       evaluated

High-income settings
  Mocroft, 1998, Archives     London, England,      1982 (a) to July
    of Internal Medicine      Chelsea and           1995
                              Westminster
                              Hospital and The
                              Royal Free Hospital

  Bacellar, 1994, Journal     Baltimore,            1985 (a) to
    of Infectious Diseases    Pittsburgh, Chicago   1993 (a)
                              and Los Angeles,
                              US, MACS cohort

  Yazdanpanah, 2001,          France, Tourcoing     January 1987 to
    International Journal     and Aquitaine         December 1995
    of Epidemiology           cohorts

  Mocroft, 1999, Journal      London, England,      1987 (a) to
    of Acquired Immune        Royal Free Center     1998 (a)
    Deficiency Syndromes      for HIV Medicine

  Moore, 1996, Annals of      Baltimore, US,        July 1989 to
    Internal Medicine         Johns Hopkins         April 1995
                              Clinical Cohort

  San-Andres, 2003,           Madrid, Spain,        January 1989 to
    Clinical Infectious       University Hospital   1997a
    Diseases

  Charurat, 2004, Journal     4 states in US and    December 1989 to
    of Women's Health         Puerto Rico, WITS     June 2002
                              Cohort

  Moorman, 1998, Journal      8 US cities, HOPS     January 1992 to
    of Acquired Immune        cohort                June 1996
    Deficiency Syndromes

  Brodt, 1997, AIDS           Frankfurt, Germany,   January 1992 to
                              Frankfurt AIDS        March 1997
                              Cohort

  Kaplan, 2000, Clinical      10 US cities,         1992 (a) to
    Infectious Diseases       Adults/Adolescents    September 1999
                              Spectrum of HIV
                              Disease (ASD) Study

  Schwarcz, 2013, AIDS        San Francisco, US,    January 1993 to
                              SFDHP                 December 2008

  Ledergerber, 1999,          7 centers in          September 1995 to
    Journal of the American   Switzerland, Swiss    March 1999
    Medical Association       HIV Cohort Study

  Mocroft, 2000, Lancet       51 centers in         December 1995 to
                              Europe, Eurosida      spring 1999 (a)
                              cohort

  Wohl, 2003, Aids Patient    10 US cities, ASD     1996 (a) to
    Care and STDs             cohort                2000 (a)

Low/middle-income settings
  Badri, 2005, The Southern   Cape Town, South      1992 (a) to
    African Journal of HIV    Africa, Cape Town     December 2000
    Medicine                  AIDS Cohort (CTAC)

  Hung, 2000, Journal of      Taiwan, National      June 1994 to
    Acquired Immune           Taiwan University     June 1999
  Deficiency Syndromes        Hospital

  Holmes, 2006, Journal of    Cape Town, South      1994 (a) to
    Acquired Immune           Africa, University    2000 (a)
    Deficiency Syndromes      of Cape Town cohort

  Podlasin, 2006, Infection   10 centers in         2000 (a) to
                              Poland                2002 (a)

  Rojanawiwat, 2011,          Lampang, Thailand,    July 2000 to
    International Health      Governmental          October 2004
                              Referral
                              Hospital (e)

First author, year, journal     Incidence rate estimate

High-income settings
  Mocroft, 1998, Archives     6.22/100 PY
    of Internal Medicine

  Bacellar, 1994, Journal     No antiretroviral nor PCP
    of Infectious Diseases    prophylaxis: 3.1/100 PY; Only
                              antiretroviral: 1.8/100 PY;
                              Antiretroviral and PCP
                              prophylaxis: 2.4/100 PY

  Yazdanpanah, 2001,          >500 cells/[mm.sup.3]: 0.4/100 PY;
    International Journal     301-500 cells/[mm.sup.3]: 0.5/100 PY;
    of Epidemiology           201-300 cells/[mm.sup.3]:1.6/100 PY;
                              101-200 cells/[mm.sup.3]: 3.1/100 PY;
                              51-100 cells/[mm.sup.3]: 6.7/100 PY;
                              >50 cells/[mm.sup.3]: 11.4/100 PY;

  Mocroft, 1999, Journal      Before 1992: 9.1/100 PY;
    of Acquired Immune        1992-1993: 5.3/100 PY; 1994:
    Deficiency Syndromes      3.5/100 PY; 1995: 6.4/100 PY;
                              1996: 4.0/100 PY; 1997: 1.9/100
                              PY

  Moore, 1996, Annals of      8.9/100 PY
    Internal Medicine

  San-Andres, 2003,           1989-1991: 5.5/100 PY; 1992:
    Clinical Infectious       5.4/100 PY; 1993: 3.5/100 PY;
    Diseases                  1994: 3.4/100 PY; 1995: 3.0/100
                              PY; 1996: 3.3/100 PY; 1997:
                              0.6/100 PY

  Charurat, 2004, Journal     Before February 1994: 0.44/100
    of Women's Health         PY March 1994 to July 1996:
                              0.86/100 PY After August 1996:
                              0.42/100 PY

  Moorman, 1998, Journal      4.6/100 PY
    of Acquired Immune
    Deficiency Syndromes

  Brodt, 1997, AIDS           1992: 17.8/100 PY; 1993: 18.2/100
                              PY; 1994: 16.3/100 PY; 1995:
                              9.9/100 PY; 1996: 6.4/100 PY

  Kaplan, 2000, Clinical      1996-1998: 4.7/100 PY (d)
    Infectious Diseases

  Schwarcz, 2013, AIDS        1993-1995: 9.5/100 PY;
                              1996-2000: 2.15/100 PY;
                              2001-2008: 0.84/100 PY

  Ledergerber, 1999,          Before ART use: 2.35/100 PY,
    Journal of the American   after ART use: 0.22/100 PY
    Medical Association

  Mocroft, 2000, Lancet       Non-ART regimens: 2.3/100 PY;
                              ART regimens: 0.5/100 PY

  Wohl, 2003, Aids Patient    US born: 3.6/100 PY; Mexican
    Care and STDs             born: 2.7/100 PY; Central
                              American born: 1.3/100 PY

Low/middle-income settings
  Badri, 2005, The Southern   1.19/100 PY
    African Journal of HIV
    Medicine

  Hung, 2000, Journal of      1995: 70.5/100 PY; 1999: 9.2/100
    Acquired Immune           PY
    Deficiency Syndromes

  Holmes, 2006, Journal of    CD4 < 50: 8.1/100 PY; CD4
    Acquired Immune           51-200: 0.6/100 PY; CD4
    Deficiency Syndromes      201-350: 0.3/100 PY; CD4 > 350: 0

  Podlasin, 2006, Infection   2000: 0.89/100 PY; 2001:
                              0.82/100 PY; 2002: 0.5/100 PY

  Rojanawiwat, 2011,          Prior to ART: 4.7/100 PY; After
    International Health      ART use: 0.3/100 PY

First author, year, journal                Notes

High-income settings
  Mocroft, 1998, Archives     Patient inclusion criteria: no CD4
    of Internal Medicine      criteria; Disease definition: considers
                              only first episode after cohort
                              enrollment

  Bacellar, 1994, Journal     Patient inclusion criteria: CD4 < 100
    of Infectious Diseases    cells/[mm.sup.3], MSM only; Disease
                              definition: considers only the first
                              episode after cohort enrollment.
                              Results stratified by use of
                              antiretroviral (b) and/or PCP
                              prophylaxis

  Yazdanpanah, 2001,          Patient exclusion criteria: patients in
    International Journal     use of antiretroviral therapy other
    of Epidemiology           than zidovudine monotheray and
                              prophylaxis; patients with less than 3
                              CD4 counts; patients with prior PCP
                              diagnosis or PCP diagnosis in the first
                              cohort visit and those in use of PCP
                              prophylaxis. Disease definition: only
                              the first case after cohort enrollment.
                              Results stratified by CD4 counts

  Mocroft, 1999, Journal      Patient inclusion criteria: no CD4
    of Acquired Immune        criteria; Disease definition: only
    Deficiency Syndromes      first ADI was considered after cohort
                              enrollment

  Moore, 1996, Annals of      Patient inclusion criteria: CD4 < 300
    Internal Medicine         cells/[mm.sup.3]; Disease definition:
                              only first episode considered after
                              cohort enrollment

  San-Andres, 2003,           Patient inclusion criteria: CD4 < 500
    Clinical Infectious       cells/[mm.sup.3] or previous diagnosis
    Diseases                  of an ADI; Disease definition: not
                              clearly stated, likely considers all
                              episodes after cohort enrollment

  Charurat, 2004, Journal     Patient inclusion criteria: no CD4
    of Women's Health         criteria, women only, without previous
                              diagnosis of AIDS; Disease definition:
                              only first episode considered after
                              cohort enrollment

  Moorman, 1998, Journal      Patient inclusion criteria: patients in
    of Acquired Immune        use of PCP prophylaxis for at least 3
    Deficiency Syndromes      months (c); Disease definition: all
                              episodes considered after cohort
                              enrollment

  Brodt, 1997, AIDS           Patient inclusion criteria: CD4 < 200
                              cells/[mm.sup.3], MSM only; Disease
                              definition: not clearly stated, likely
                              considers all episodes after cohort
                              enrollment

  Kaplan, 2000, Clinical      Patient inclusion criteria: no CD4
    Infectious Diseases       criteria; Disease definition: not
                              clearly stated, likely considers all
                              episodes after cohort enrollment

  Schwarcz, 2013, AIDS        Patient inclusion criteria: no CD4
                              criteria; Disease definition: considers
                              only the first episode after cohort
                              enrollment

  Ledergerber, 1999,          Patient inclusion criteria: no CD4
    Journal of the American   criteria, patients who started ART
    Medical Association       between September 1995 and December
                              1997. Disease definition: only first
                              episode considered after cohort
                              enrollment

  Mocroft, 2000, Lancet       Patient inclusion criteria: CD4 < 500
                              cells/[mm.sup.3]; Disease definition:
                              considers the first episode after
                              cohort enrollment

  Wohl, 2003, Aids Patient    Patient inclusion criteria: no CD4
    Care and STDs             criteria; included US born Latinos,
                              Mexican born Latinos and Central
                              American Latinos. Disease definition:
                              not clear stated, apparently included
                              all episodes presented in the study
                              period

Low/middle-income settings
  Badri, 2005, The Southern   Patient inclusion criteria: no CD4
    African Journal of HIV    criteria; Disease definition: not
    Medicine                  clearly stated, likely considers all
                              episodes after cohort enrollment

  Hung, 2000, Journal of      Patient inclusion criteria: no CD4
    Acquired Immune           criteria; Disease definition: considers
    Deficiency Syndromes      only the first episode after cohort
                              enrollment

  Holmes, 2006, Journal of    Patient inclusion criteria: patients
    Acquired Immune           with at least two CD4 cell counts;
    Deficiency Syndromes      Disease definition: WHO stage III and
                              IV, considers only first episode
                              considered after cohort enrollment.
                              Results were stratified by CD4

  Podlasin, 2006, Infection   Patient inclusion criteria: none;
                              Disease definition: not clearly stated,
                              likely considers all episodes after
                              cohort enrollment

  Rojanawiwat, 2011,          Patient inclusion criteria: none;
    International Health      Disease definition: not clearly stated,
                              likely considers the first episode
                              after cohort enrollment

ADI: AIDS defining illness; ART: highly active antiretroviral
therapy; MSM: men who have sex with men; PCP: Pneumocytis carinii
pneumonia.

(a) Month not specified.

(b) Zidovudine, didanosine or both.

(c) PCP prophylaxis was prescribed for patients with CD4 count less
than 200 cells/[mm.sup.3] or considered at risk by their clinicians
(even if CD4 > 200 cells/[mm.sup.3]).

(d) Results for other years shown in figure format only, thus not
reported here.

(e) In 2002 the government introduced the co-formulation stavudine,
lamivudine and nevirapine (on a pilot basis). The use of this
medication gradually increased especially after 2004.

Table 3--Incidence rates for cerebral toxoplasmosis among
HIV-infected individuals from high and low/middle-income settings.

First author, year,           Setting and cohort      Time period
journal                       (when applicable)       evaluated

High-income settings
  Bacellar, 1994, Journal     Baltimore,              1985 (a) to
    of Infectious Diseases    Pittsburgh, Chicago     1993 (a)
                              and Los Angeles, US,
                              MACS cohort

  Yazdanpanah, 2001,          France, Tourcoing       January 1987 to
    International Journal     and Aquitaine           December 1995
    of Epidemiology           cohorts

  Moore, 1996, Annals of      Baltimore, US, Johns    July 1989 to
    Internal Medicine         Hopkins Clinical        April 1995
                              Cohort

  San-Andres, 2003,           Madrid, Spain,          January 1989 to
    Clinical Infectious       University Hospital     1997 (a)
    Diseases

  Sacktor, 2001, Neurology    Baltimore,              January 1990 to
                              Pittsburgh, Chicago     December 1998
                              and Los Angeles, US,
                              MACS cohort

  Brodt, 1997, AIDS           Frankfurt, Germany,     January 1992 to
                              Frankfurt AIDS          March 1997
                              Cohort

  Ledergerber, 1999,          7 centers in            September 1995
    Journal of the American   Switzerland, Swiss      to March 1999
    Medical Association       HIV Cohort Study

  Wohl, 2003, Aids Patient    10 US cities, ASD       1996 (a) to
    Care and STDs             cohort                  2000 (a)

  Garvey, 2011, European      10 UK HIV centers,      January 1996 to
    Journal of Neurology      CHIC (UK                December 2007
                              Collaborative HIV
                              Cohort)

  Riveiro-Barciela, 2013,     Barcelona, Spain        January 2000 to
    HIV medicine                                      December 2010

Low/middle-income settings
  Badri, 2005, The Southern   Cape Town, South        1992 (a) to
    African Journal of HIV    Africa, Cape Town       December 2000
    Medicine                  AIDS Cohort (CTAC)

  Holmes, 2006, Journal of    Cape Town, South        1994 (a) to
    Acquired Immune           Africa, University of   2000 (a)
    Deficiency Syndromes      Cape Town cohort

  Rojanawiwat, 2011,          Lampang, Thailand,      July 2000 to
    International Health      Governmental Referral   October 2004
                              Hospital (c)

First author, year,               Incidence rate estimate
journal

High-income settings
  Bacellar, 1994, Journal     No antiretroviral nor PCP
    of Infectious Diseases    prophylaxis: 6.9/100 PY; Only
                              antiretroviral: 6.0/100 PY;
                              Antiretroviral and PCP
                              prophylaxis: 14.8/100 PY

  Yazdanpanah, 2001,          >500 cells/[mm.sup.3]: 0.1/100 PY;
    International Journal     301-500 cells/[mm.sup.3]: 0.6/100 PY;
    of Epidemiology           201-300 cells/[mm.sup.3]: 1.1/100 PY;
                              101-200 cells/[mm.sup.3]: 2.0/100 PY;
                              51-100 cells/[mm.sup.3]: 3.9/100 PY;
                              >50 cells/[mm.sup.3]: 12.6/100 PY

  Moore, 1996, Annals of      2.3/100 PY
    Internal Medicine

  San-Andres, 2003,           1989-1991: 2.1/100 PY, 1992:
    Clinical Infectious       2.9/100 PY, 1993: 2.4/100 PY,
    Diseases                  1994: 0.8/100 PY, 1995: 1.1/100
                              PY, 1996: 1.0/100 PY, 1997:
                              1.8/100 PY

  Sacktor, 2001, Neurology    1990-1992: 0.54/100 PY,
                              1993-1995: 0.38/100 PY,
                              1996-1998: 0.22/100 PY

  Brodt, 1997, AIDS           1992: 10.6/100 PY, 1993: 6.1/100
                              PY, 1994: 3.9/100 PY, 1995:
                              4.0/100 PY, 1996: 2.6/100 PY

  Ledergerber, 1999,          Before ART use: 1.45/100 PY,
    Journal of the American   after ART use: 0.18/100 PY
    Medical Association

  Wohl, 2003, Aids Patient    US born: 0; Mexican born:
    Care and STDs             0.5/100 PY; Central American
                              born: 0.7/100 PY

  Garvey, 2011, European      Total: 0.12/100 PY; 1996-1997:
    Journal of Neurology      0.32/100 PY, 1998-1999: 0.11/100
                              PY, 2000-2001: 0.15/100 PY,
                              2002-2003: 0.11/100 PY, 2004-2005:
                              0.09/100 PY, 2006-2007: 0.04/100 PY

  Riveiro-Barciela, 2013,     2000 to June 2005: 0.32/100 PY;
    HIV medicine              July 2005-2010: 0.11/100 PY

Low/middle-income settings
  Badri, 2005, The Southern   0.15/100 PY
    African Journal of HIV
    Medicine

  Holmes, 2006, Journal of    CD4 < 50: 1.2/100 PY; CD4
    Acquired Immune           51-200: 0; CD4 201-350: 0;
    Deficiency Syndromes      CD4 > 350: 0

  Rojanawiwat, 2011,          Before ART use: 1.2/100 PY,
    International Health      After ART use: 1.0/100 PY

First author, year,                          Notes
journal

High-income settings
  Bacellar, 1994, Journal     Patient inclusion criteria: CD4 < 100
    of Infectious Diseases    cells/[mm.sup.3], MSM only; Disease
                              definition: considers only the first
                              episode after cohort enrollment.
                              Results stratified by use of
                              antiretroviral (b) and/or PCP
                              prophylaxis

  Yazdanpanah, 2001,          Patient exclusion criteria:patients in
    International Journal     use of antiretroviral therapy other
    of Epidemiology           than zidovudine monotheray and
                              prophylaxis; patients with less than 3
                              CD4 counts; patients with prior NTX
                              diagnosis or with NTX diagnosis in the
                              first cohort visit and those in use of
                              NTX prophylaxis. Disease definition:
                              only the first case after cohort
                              enrollment. Results stratified by CD4
                              counts

  Moore, 1996, Annals of      Patient inclusion criteria: CD4 < 300
    Internal Medicine         cells/[mm.sup.3]; Disease definition:
                              considers only the first episode after
                              cohort enrollment

  San-Andres, 2003,           Patient inclusion criteria: CD4 < 500
    Clinical Infectious       cells/[mm.sup.3] or previous diagnosis
    Diseases                  of AIDS; Disease definition: not
                              clearly stated, likely considers all
                              episodes after cohort enrollment

  Sacktor, 2001, Neurology    Patient inclusion criteria: no CD4
                              criteria, MSM only; Disease definition:
                              not clearly stated, likely considers
                              all episodes after cohort enrollment

  Brodt, 1997, AIDS           Patient inclusion criteria: CD4 < 200
                              cells/[mm.sup.3], MSM only; Disease
                              definition: not clearly stated, likely
                              considers all episodes after cohort
                              enrollment

  Ledergerber, 1999,          Patient inclusion criteria: no CD4
    Journal of the American   criteria, patients who started ART
    Medical Association       between September 1995 and December
                              1997. Disease definition: considers
                              only the first episode after cohort
                              enrollment

  Wohl, 2003, Aids Patient    Patient inclusion criteria: no CD4
    Care and STDs             criteria; included US born Latinos,
                              Mexican born Latinos and Central
                              American Latinos. Disease definition:
                              not clear stated, likely considers all
                              episodes presented in the study period

  Garvey, 2011, European      Patient inclusion criteria: none;
    Journal of Neurology      Disease definition: considers only the
                              first episode after cohort enrollment

  Riveiro-Barciela, 2013,     Patient inclusion criteria: none;
    HIV medicine              Disease definition: not clearly stated,
                              likely considers all episodes after
                              cohort enrollment

Low/middle-income settings
  Badri, 2005, The Southern   Patient inclusion criteria: no CD4
    African Journal of HIV    criteria; Disease definition: not
    Medicine                  clearly stated, likely considers all
                              episodes after cohort enrollment

  Holmes, 2006, Journal of    Patient inclusion criteria: patients
    Acquired Immune           with at least two CD4 cell counts;
    Deficiency Syndromes      Disease definition: WHO stage III and
                              IV; considers only first episode after
                              cohort enrollment. Results were
                              stratified by CD4

  Rojanawiwat, 2011,          Patient inclusion criteria: none;
    International Health      Disease definition: not clearly stated,
                              likely considers all episodes after
                              cohort enrollment

ART: highly active antiretroviral therapy; MSM: men who have sex
with men; NTX: Cerebral toxoplasmosis; PCP: Pneumocytis carinii
pneumonia.

(a) Month not specified.

(b) Zidovudine, didanosine or both.

(c) In 2002 the government introduced the co-formulation stavudine,
lamivudine and nevpilot basis). The use of this medication gradually
increased especially after 2004.

Table 4--Incidence rate of Mycobacterium avium complex among
HIV-infected individuals from high and low/middle-income settings.

First author, year,          Setting and cohort      Time period
journal                      (when applicable)       evaluated

High-income settings
  Bacellar, 1994, Journal    Baltimore,              1985 (a) to
    of Infectious Diseases   Pittsburgh, Chicago     1993 (a)
                             and Los Angeles, US,
                             MACS cohort

  Chaisson, 1992, American   Multicenter             April 1987 to
    review of respiratory    observational cohort    1990 (c)
    disease                  in US

  Yazdanpanah, 2001,         France, Tourcoing       January 1987 to
    International Journal    and Aquitaine           December 1995
    of Epidemiology          cohorts

  Mocroft, 1999, Journal     London, England,        1987 (c) to
    of Acquired Immune       Royal Free Center for   1998 (c)
    Deficiency Syndromes     HIV Medicine

  Moore, 1996, Annals of     Baltimore, US, Johns    July 1989 to
    Internal Medicine        Hopkins Clinical        April 1995
                             Cohort

  San-Andres, 2003,          Madrid, Spain,          January 1989 to
    Clinical Infectious      University Hospital     1997 (c)
    Diseases

  Charurat, 2004, Journal    4 states in US and      December 1989 to
    of Women's Health        Puerto Rico, WITS       June 2002
                             Cohort

  Rossi, 2001, Swiss         7 centers in            January 1990 to
    Medical Weekly           Switzerland, Swiss      December 1999
                             HIV Cohort Study

  Brodt, 1997, AIDS          Frankfurt, Germany,     January 1992 to
                             Frankfurt AIDS          March 1997
                             Cohort

  Kaplan, 2000, Clinical     10 US cities,           1992 (c) to
    Infectious Diseases      Adults/Adolescents      September 1999
                             Spectrum of HIV
                             Disease (ASD) Study

  Schwarcz, 2013, AIDS       San Francisco, US,      January 1993 to
                             SFDHP                   December 2008

  Kirk, 2000, American       17 European             May 1994 to
    Journal of Respiratory   countries, EuroSIDA     February 1999
    and Critical Care        Cohort
    Medicine

  Mocroft, 2000, Lancet      51 centers in Europe,   May 1994 to
                             Eurosida cohort         spring 1999 (c)

  Baril, 2000, AIDS          Paris, France,          January 1995 to
                             Pitie-Salpetriere       December 1997
                             Hospital

  Ledergerber, 1999,         7 centers in            September 1995
    Journal of the           Switzerland, Swiss      to March 1999
    American Medical         HIV Cohort Study
    Association

  Wohl, 2003, Aids Patient   10 US cities, ASD       1996 (c) to
    Care and STDs            cohort                  2000 (c)

Low/middle-income settings

  Badri, 2005, The           Cape Town, South        1992 (c) to
    Southern African         Africa, Cape Town       December 2000
    Journal of HIV           AIDS Cohort (CTAC)
    Medicine

  Bonard, 2004, AIDS         Ivory Coast, Cotrame    1992 (c) to
                             ANRS 1203               October 2002

  Gadelha, 2002, The         Rio de Janeiro,         September 1997
    Brazilian Journal of     Brazil, IPEC cohort     to December 1999
    Infectious Diseases

First author, year,                Incidence rate estimate
journal

High-income settings
  Bacellar, 1994, Journal    No antiretroviral nor PCP prophylaxis:
    of Infectious Diseases   6.9/100 PY; Only antiretroviral: 6.0/100
                             PY; Antiretroviral and PCP prophylaxis:
                             14.8/100 PY

  Chaisson, 1992, American   8.6/100 PY
    review of respiratory
    disease

  Yazdanpanah, 2001,         >500 cells/[mm.sup.3]: 0.0/100 PY; 301-
    International Journal    500 cells/[mm.sup.3]: 0.2/100 PY; 201-
    of Epidemiology          300 cells/[mm.sup.3]: 0.3/100 PY; 101-
                             200 cells/[mm.sup.3]: 1.0/100 PY; 51-100
                             cells/[mm.sup.3]: 1.9/100 PY; >50
                             cells/[mm.sup.3]: 9.5/100 PY

  Mocroft, 1999, Journal     Before 1992: 1.1/100 PY, 1992-1993:
    of Acquired Immune       3.8/100 PY, 1994: 4.1/100 PY, 1995:
    Deficiency Syndromes     4.1/100 PY, 1996: 2.7/100 PY, 1997:
                             1.0/100 PY

  Moore, 1996, Annals of     7.4/100 PY
    Internal Medicine

  San-Andres, 2003,          1989-1991: 1.5/100 PY, 1992: 2.9/100 PY,
    Clinical Infectious      1993: 1.5/100 PY, 1994: 1.1/100 PY,
    Diseases                 1995: 1.9/100 PY, 1996: 2.5/100 PY,
                             1997: 0.6/100 PY

  Charurat, 2004, Journal    Before February 1994: 0.32/100 PY; March
    of Women's Health        1994 to July 1996: 0.23/100 PY; After
                             August 1996: 0.12/100 PY

  Rossi, 2001, Swiss         Overall: 5.8/100 PY, 1990-1996: 8.8/100
    Medical Weekly           PY, 1997-1999: 1.4/100 PY

  Brodt, 1997, AIDS          1992: 4.5/100 PY; 1993: 6.1/100 PY;
                             1994: 6.6/100 PY; 1995: 5.4/100 PY;
                             1996: 2.8/100 PY;

  Kaplan, 2000, Clinical     1996-1998: 3.4/100 PY (e)
    Infectious Diseases

  Schwarcz, 2013, AIDS       1993-1995: 8.52/100 PY; 1996-2000:
                             1.34/100 PY; 2001-2008: 0.32/100 PY

  Kirk, 2000, American       1.38/100 PY
    Journal of Respiratory
    and Critical Care
    Medicine

  Mocroft, 2000, Lancet      Non-ART regimens: 2.3/100 PY; ART
                             regimens: 0.5/100 PY

  Baril, 2000, AIDS          January 1996 to June 1996: 13.4/100 PY;
                             July 1996 to December 1997: 2.6/100 PY

  Ledergerber, 1999,         Before ART use: 1.79/100 PY; after ART
    Journal of the           use: 0.76/100 PY
    American Medical
    Association

  Wohl, 2003, Aids Patient   US born: 1.8/100 PY; Mexican born:
    Care and STDs            1.1/100 PY; Central American born:
                             0.4/100 PY
Low/middle-income settings

  Badri, 2005, The           0.40/100 PY
    Southern African
    Journal of HIV
    Medicine

  Bonard, 2004, AIDS         1.85/100 PY

  Gadelha, 2002, The         0
    Brazilian Journal of
    Infectious Diseases

First author, year,                       Notes
journal

High-income settings
  Bacellar, 1994, Journal    Patient inclusion criteria: CD4 < 100
    of Infectious Diseases   cells/[mm.sup.3], MSM only; Disease
                             definition: CDC 1993; considers only the
                             first episode of each ADI after cohort
                             enrollment. Results stratified by use of
                             antiretroviral (b) and/or PCP
                             prophylaxis

  Chaisson, 1992, American   Patient inclusion criteria: patients
    review of respiratory    with AIDS diagnoses defined by PCP, an
    disease                  opportunistic disease other than PCP and
                             CD4 < 250 cells/[mm.sup.3], or AIDS
                             related complex and CD4 < 250 cells/
                             [mm.sup.3]; Disease definition: not
                             clearly stated, likely considers only
                             the first episodes after cohort
                             enrollment

  Yazdanpanah, 2001,         Patient exclusion criteria: patients in
    International Journal    use of antiretroviral therapy other than
    of Epidemiology          zidovudine monotheray and prophylaxis;
                             patients with less than 3 CD4 counts;
                             excluded patients with prior MAC
                             diagnosis or with MAC diagnosis in the
                             first cohort visit and those in use of
                             MAC prophylaxis. Disease definition:
                             considers only the first case after
                             cohort enrollment. Results stratified by
                             CD4 counts

  Mocroft, 1999, Journal     Patient inclusion criteria: no CD4
    of Acquired Immune       criteria; Disease definition: considers
    Deficiency Syndromes     only the first episode after cohort
                             enrollment

  Moore, 1996, Annals of     Patient inclusion criteria: CD4 < 300
    Internal Medicine        cells/[mm.sup.3]; Disease definition:
                             considers only the first episode after
                             cohort enrollment

  San-Andres, 2003,          Patient inclusion criteria: CD4 < 500
    Clinical Infectious      cells/[mm.sup.3] or previous diagnosis
    Diseases                 AIDS; Disease definition: not clearly
                             stated, likely considers all episodes
                             after cohort enrollment

  Charurat, 2004, Journal    Patient inclusion criteria: no CD4
    of Women's Health        criteria, women only, without previous
                             diagnosis of AIDS; Disease definition:
                             considers only the first episode after
                             cohort enrollment (d)

  Rossi, 2001, Swiss         Patient inclusion criteria: CD4 < 50
    Medical Weekly           cells/[mm.sup.3]; Disease definition:
                             considers only the first episode after
                             cohort enrollment

  Brodt, 1997, AIDS          Patient inclusion criteria: CD4 < 200
                             cells/[mm.sup.3], MSM only; Disease
                             definition: not clearly stated, likely
                             considers all episodes after cohort
                             enrollment

  Kaplan, 2000, Clinical     Patient inclusion criteria: no CD4
    Infectious Diseases      criteria; Disease definition: not
                             clearly stated, likely considers all
                             episodes after cohort enrollment

  Schwarcz, 2013, AIDS       Patient inclusion criteria: no CD4
                             criteria; Disease definition: considers
                             only the first episode after cohort
                             enrollment

  Kirk, 2000, American       Patient inclusion criteria: no CD4
    Journal of Respiratory   criteria; Disease definition: considers
    and Critical Care        only the first episode after cohort
    Medicine                 enrollment

  Mocroft, 2000, Lancet      Patient inclusion criteria: CD4 < 500
                             cells/[mm.sup.3]; Disease definition:
                             considers only the first episode after
                             cohort enrollment

  Baril, 2000, AIDS          Patient inclusion criteria: no CD4
                             criteria; Disease definition: considers
                             the first episode after cohort
                             enrollment

  Ledergerber, 1999,         Patient inclusion criteria: no CD4
    Journal of the           criteria, patients who started ART
    American Medical         between September 1995 and December
    Association              1997. Disease definition: considers only
                             the first episode after cohort
                             enrollment (d)

  Wohl, 2003, Aids Patient   Patient inclusion criteria: no CD4
    Care and STDs            criteria; included US born Latinos,
                             Mexican born Latinos and Central
Low/middle-income settings   American Latinos. Disease definition:
                             not clear stated, apparently included
                             all OI presented in the study period

  Badri, 2005, The           Patient inclusion criteria: no CD4
    Southern African         criteria; Disease definition:
    Journal of HIV           disseminated atypical mycobacteria;
    Medicine                 likely considers all episodes after
                             cohort enrollment

  Bonard, 2004, AIDS         Patient inclusion criteria: no CD4
                             criteria; Disease definition: considers
                             only the first episode after cohort
                             enrollment (d)

  Gadelha, 2002, The         Patient inclusion criteria: CD4 < 100
    Brazilian Journal of     cells/[mm.sup.3]; Excluded patients
    Infectious Diseases      under MAC treatment or prophylaxis.
                             Disease definition: considers only the
                             first episode presented in the study
                             period

ART: highly active antiretroviral therapy; MAC: Mycbacterium avium
complex; MSM: men who have sex with men; PCP: Pneumocystis carinii
pneumonia.

(a) Time inferred from information contained in the text.

(b) Zidovudine, didanosine or  both.

(c) Month not specified.

(d) Classify as Mycobacterium non tuberculosis.

(e) Results for other years shown in figure format only, thus not
reported here.
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Author:Coelho, Lara; Veloso, Valdilea Goncalves; Grinsztejn, Beatriz; Luz, Paula Mendes
Publication:The Brazilian Journal of Infectious Diseases
Article Type:Report
Geographic Code:3BRAZ
Date:Mar 1, 2014
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