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Table 5 Immunological research of co-infection between TB and parasitic diseases

From: Co-infection of tuberculosis and parasitic diseases in humans: a systematic review

Country

Year of report

Tuberculosis

Parasitic disease/species

Subject

Conclusions

No. of reference

France

2003

PTB

American cutaneous leishmaniasis

A 44-year-old man with triple infection of cutaneous leishmaniasis, lepromatous leprosy, and PTB

Unresponsiveness to IL-12 of patient’s T cells after stimulation with Leishmania guyanensis, M. bovis bacille Calmette-Guerin, and M. leprae antigens suggested the inability to mount an appropriate Th cell response to upregulate the IL-12 receptor expression.

[14]

Gambia

1999

M. TB

Malaria

Review

Malarial parasites can decrease their vertebrate host’s effective humoral and cellular immune responses to M. TB.

[35]

USA

2004

M. TB

Plasmodium yoelii NL

Mice

Co-infected mice were less able to contain growth of M. TB in lung, spleen, and liver and had increased mortality.

[36]

Thailand

2006

M. TB

Plasmodium falciparum

HSP70 (M. TB) and ATPBP (Plasmodium falciparum)

HSP70 and ATPBP share a common molecular function as ATP binding resulting from purine nucleotide binding. Therefore, a competitive antagonist effect between both molecules can be expected.

[37]

Germany

2012

M. TB

Plasmodium berghei NK65

An experimental mouse model of co-infection

Co-infection exacerbated chronic TB while rendering mice less refractory to Plasmodium. Co-infected animals presented with enhanced inflammatory immune responses as reflected by exacerbated leukocyte infiltrates, tissue pathology and hypercytokinemia accompanied by altered T-cell responses.

[38]

Unknown

1989

PTB

Opisthorchiasis

173 patients with PTB complicated by opisthorchiasis

Among them, activity of the α1-proteinase inhibitor was more frequently higher and carriers of two markers i.e. Hp 2–2 and Gc 1–1 were more frequent.

[39]

Unknown

1992

PTB

Opisthorchiasis

12 PTB patients concurrent with opisthorchiasis

When the course of TB is aggravated by opisthorchiasis invasion, the number of cases of antibacterial therapy intolerance increases and prognosis of the diseases deteriorates. It was shown that the antibacterial and anthelminthic therapy had a favourable clinical and immunologic effect.

[40]

Unknown

1992

M. TB

Opisthorchiasis

Animal

In comparison with the groups of animals with monoinvasion and monoinfection, at the acute invasive phase of mixed pathology (2 weeks) the activity of the host’s immune system increases, while the biological activities of both pathogens decrease; however, at the subacute phase (2.5 months), all were contrary respectively.

[41]

Russia

2003

TB

Opisthorchiasis

Golden hamsters with SRBC parasitocenosis

In cases of mixed pathology, at the acute stage of invasion, the immune system showed increased responses with respect to specific and heterologous antigens; in the chronization of invasion the formation of antibodies to heterologous antigens (SRBC) and the level of specific antiopisthorchiasis and anti-TB immune responses decreased together.

[42]

China

2009

PTB

Echinococcosis

A 18 years old male and a 36 years female

As the echinococcosis chronicity increased, the immune profile in both subjects changed from a Th1 to Th2 response. Such an elevated Th2 immune profile, with subsequent suppression of the Th1 immune response, is a common feature of chronic helminth infections.

[27]

USA

2012

M. TB

Litomosoides sigmodontis

Cotton rats with chronic L. sigmodontis infection and uninfected controls were challenged with M. TB by intranasal inoculation.

Chronic filarial infections do not exacerbate M. TB infection in the cotton rat model. It may be possible to develop worm-derived therapies for autoimmune diseases that do not substantially increase the risk for infections.

[43]

USA

2012

M. TB

Filarial infections

Review

Filarial infections very clearly alter the magnitude and quality of the mycobacteria-specific cytokine responses, responses that have been typically associated with control of these intracellular pathogens.

[44]

Denmark

2007

TB

Intestinal helminth

Review

Co-infections cause a range of immunomodulation characterized by enhanced Th2-type cytokine profiles, high IgE levels and upregulated regulatory T-cell activity, as well as chronic immune activation.

[45]

Brazil

2007

PTB

Intestinal helminth

40 PTB patients and 25 healthy controls

Compared to either TB patients or healthy controls, co-infected patients’ absolute frequencies of CD3+, CD4+, CD8+, NK T cell and CD4+CD25high T cell increased. Differences in CD4 T cell frequencies were accompanied by lower IFN-γ and elevated and sustained IL-10 levels in WB cultures from co-infected patients compared to TB patients.

[46]

Mexico

2012

TB

Helminthic infections

Review

Helminths very clearly alter the magnitude of the mycobacteria-specific cytokine responses, altering the control of the mycobacteria growth. Mycobacteria-induced immune responses are suppressed by helminth infections.

[47]

USA

2012

TB

Helminths

Review

Helminth-induced Th2 and T reg responses impinge on host resistance against M. TB infection. Th1 response is reduced in helminth co-infected hosts. Helminth-induced alternatively activated macrophages contribute to enhanced susceptibility to TB.

[48]

Brazil

2002

BCG vaccination

Ascaris lumbricoides, Entamoeba histolytica, and Strongyloides stercoralis

14 male students aged 12–15 years: 7 having protozoan or helminthic infections and 7 free of intestinal parasites

Th2-like IL-10 responses induced by intestinal parasites may interfere in BCG-induced Th1-like IFN-γ response. Intestinal parasitic infections may significantly alter the protective immune response to BCG vaccination.

[49]

Sweden

2005

BCG vaccination to protect against M. TB

S. mansoni

BCG vaccinated mice with prior S. mansoni infection

S. mansoni infection reduces the protective efficacy of BCG vaccination against M. TB possibly by attenuation of protective immune responses to mycobacterial antigens and/or by polarizing the general immune responses to the Th2 profile.

[50]

USA

2011

TB vaccines in protecting against M. TB

Plasmodium yoelii NL

TB vaccines in a co-infection mouse model of two pathogens

The effectiveness of novel TB vaccines in protecting against TB was unaffected by a primary malaria co-infection in a mouse model of PTB.

[51]

  1. Abbreviations: PTB = pulmonary tuberculosis; M. leprae = mycobacterium leprae; M. TB = mycobacterium tuberculosis; SRBC = sheep red blood cells; IL = interleukin; Th = T helper; Treg = T regulatory; NL = non-lethal; HSP = heat shock protein; ATP = adenosine triphosphate; ATPBP = ATP-binding protein; Ig = immunoglobulin; CD = cluster of differentiation; NK = natural killer; IFN = interferon; WB = whole blood; BCG = Bacillus Calmette-Guerin; L. sigmodontis = litomosoides sigmodontis; S. mansoni = schistosoma mansoni.