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Bhengu, K.N.;  Naidoo, P.;  Singh, R.;  Mpaka-Mbatha, M.N.;  Nembe, N.;  Duma, Z.;  Pillay, R.;  Mkhize-Kwitshana, Z.L. Immunological Interactions between Intestinal Helminth Infections and Tuberculosis. Encyclopedia. Available online: https://encyclopedia.pub/entry/34909 (accessed on 06 July 2024).
Bhengu KN,  Naidoo P,  Singh R,  Mpaka-Mbatha MN,  Nembe N,  Duma Z, et al. Immunological Interactions between Intestinal Helminth Infections and Tuberculosis. Encyclopedia. Available at: https://encyclopedia.pub/entry/34909. Accessed July 06, 2024.
Bhengu, Khethiwe Nomcebo, Pragalathan Naidoo, Ravesh Singh, Miranda N. Mpaka-Mbatha, Nomzamo Nembe, Zamathombeni Duma, Roxanne Pillay, Zilungile L. Mkhize-Kwitshana. "Immunological Interactions between Intestinal Helminth Infections and Tuberculosis" Encyclopedia, https://encyclopedia.pub/entry/34909 (accessed July 06, 2024).
Bhengu, K.N.,  Naidoo, P.,  Singh, R.,  Mpaka-Mbatha, M.N.,  Nembe, N.,  Duma, Z.,  Pillay, R., & Mkhize-Kwitshana, Z.L. (2022, November 16). Immunological Interactions between Intestinal Helminth Infections and Tuberculosis. In Encyclopedia. https://encyclopedia.pub/entry/34909
Bhengu, Khethiwe Nomcebo, et al. "Immunological Interactions between Intestinal Helminth Infections and Tuberculosis." Encyclopedia. Web. 16 November, 2022.
Immunological Interactions between Intestinal Helminth Infections and Tuberculosis
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This entry is adapted from the peer-reviewed paper 10.3390/diagnostics12112676

Helminth infections are among the neglected tropical diseases affecting billions of people globally, predominantly in developing countries. Helminths’ effects are augmented by coincident tuberculosis disease, which infects a third of the world’s population. The role of helminth infections on the pathogenesis and pathology of active tuberculosis (T.B.) remains controversial. Parasite-induced suppression of the efficacy of Bacille Calmette-Guerin (BCG) has been widely reported in helminth-endemic areas worldwide. T.B. immune response is predominantly proinflammatory T-helper type 1 (Th1)-dependent. On the other hand, helminth infections induce an opposing anti-inflammatory Th2 and Th3 immune-regulatory response. 

Mycobacterium tuberculosis helminths coinfection immune response Bacille Calmette-Guerin vaccination

1. Introduction

Intestinal helminths are parasitic worms infecting over 1.5 billion people globally [1] Most helminth cases occur in tropical and sub-tropical areas such as Sub-Saharan Africa, the Americas, China and East Asia [1]. Humans are infected with helminth parasites after ingesting eggs or larvae from contaminated water, soil or food or through active skin penetration by infective hookworm larvae in contaminated soil [2]. Climate change, malnutrition, overcrowding, poverty and poor sanitary conditions are risk factors associated with the high helminth prevalence in Africa and other developing countries, making effective treatment and the eradication of infection challenging [1][2][3][4]. The most common intestinal helminth species infecting humans are Schistosoma mansoni, Trichuris trichuria (whipworm), Ascaris lumbricoides (roundworm), Necator americanus and Ancylostoma duodenale (hookworms) [1][2].
Tuberculosis (T.B.) is an infectious bacterial disease caused by different strains of acid-fast bacilli belonging to the Mycobacterium tuberculosis (Mtb) complex [5]. The T.B. bacteria are airborne, and transmission occurs when a T.B.-infected person coughs, sneezes or spits, expelling the infected droplets into the air. Inhalation of these aerosols may result in infection of the next host [6]. T.B. continues to be a public health problem across the world, with the World Health Organization (WHO) reporting over 10 million T.B. cases in 2020 [7]. Approximately 1.5 million TB-related deaths were reported worldwide in 2020 [7]. Globally, Africa accounts for 50% of cases of T.B. and human immunodeficiency virus (HIV) coinfection [7]. Furthermore, in Africa, T.B. is commonly observed in HIV-infected patients, and it is the leading cause of death among them [7].
T.B. exposure results in the initiation of an immune response to fight the infection. The immune response to T.B. involves the interaction of innate and adaptive immune responses. It is dependent on the cellular immune response, which is mediated by proinflammatory T-helper type 1 (Th1) and Th17 cells [8][9][10]. The Th1 cytokines, which are interferon-γ (IFN-γ), interleukin 12 (IL12) and tumor necrosis factor-α (TNF-α) and Th17 cytokines (IL-17, IL-21, IL-22 and IL-23) play a role in combating bacterial and viral infections [8][9][10]. Helminth exposure, on the other hand, induces an anti-inflammatory Th2 immune response which is characterized by the production of cytokines such as IL-4, IL-5, IL-9, IL-10 and IL-13, and increased levels of circulating immunoglobulin E (IgE) antibodies, eosinophils, and mast cells, regulatory T cells (Tregs) and transforming growth factor-β (TGF-β) [11][12].
T.B. commonly overlaps geographically with soil-transmitted helminths, especially in developing countries [13][14][15][16], and this co-endemicity has implications for public health and the afflicted hosts. Helminth infection-induced immune responses could promote the pathogenesis of severe T.B. infections [16][17][18]; others report that they can also be beneficial in reducing T.B. severity [19][20][21][22]. However, there is no conclusive evidence to confirm whether helminth-induced immunity modulates T.B.-specific immune responses or vice-versa, and studies have yielded contradictory results. Therefore, knowledge on the interaction between T.B. and helminth infections is limited, as are the available data.

2. Host Immune Response during Helminth Coinfection with T.B.

The geographic distributions of helminths and T.B. overlap substantially, particularly in underdeveloped countries, resulting in an increased likelihood of coinfection with both pathogens [15][16]. This coexistence has also led to the hypothesis that helminths can worsen the effects of T.B. There have been suggestions that the anti-inflammatory response induced by helminths in cases of coinfection might dampen protective and immunopathological responses to T.B. [15][16].
An Ethiopian study investigated the association between intestinal helminths and active T.B. and found that helminth infection increases the likelihood of developing active T.B. [23]. This and other studies also suggested that patients with coinfection may have antagonistic effector cell responses in responding to and regulating these diseases [24][25]. This can also imply that the efficacy of the vaccines may be reduced.
One school of thought suggests that helminths create an environment that weakens the host’s defenses against T.B. By activating the IL-4 receptor pathway, a preexisting helminth infection inhibits an innate pulmonary anti-T.B. defense [26]. In coinfected mice models, helminth-induced lung alterations increased susceptibility to T.B. [26]. Macrophages can be classically or alternatively activated. Classically activated macrophages (CAMs) increase the activity of nitric oxide synthase (iNOS), which converts L-arginine to nitric oxide and citrulline. Nitric oxide promotes intracellular Mtb killing.
On the other hand, alternatively activated macrophages (AAMs) induce arginase, which competes with iNOS for L-arginine, thereby reducing nitric oxide production for the intracellular killing of Mtb [27]. Mtb resistance in helminth-infected mice is promoted by AAMs. This major cellular pathway compromises the helminth-infected host’s ability to limit Mtb growth [26].
A review in support of this proposed role of the Th2-dominant phenotype on Mtb control illustrated that AAMs might inhibit the macrophage killing of Mtb [27]. Conversely, a murine study in South Africa using Nippostrongylus brasiliensis (Nb) revealed that Mtb colonies were reduced in the lungs of Nb-infected mice. The stimulation of pulmonary CD4+ T cells and Th1 and Th2 cytokines, neutrophils and alveolar macrophages was elevated. This suggests that Nb infection triggers a macrophage response, which protects the host throughout the early phases of mycobacterial disease and subsequent illness [19].
Both helminths and T.B. have independent mechanisms for initiating the host immune response, with significant consequences for the immunology of each infection [15][16]. The coexistence of helminth infection and active tuberculosis has been demonstrated in epidemiological, cross-sectional and case-control studies that looked at the prevalence and correlation of the two diseases. Pulmonary T.B. patients were found to have a significant rate of intestinal nematode infection, indicating that helminth immunomodulation may affect the control of T.B. [23][28].
In Ethiopia, some studies reported an increase in the prevalence of helminth coinfection in T.B. patients, where one study found a higher risk of parasites among active T.B. patients than in healthy community controls [17][29][30]. Likewise, in Iran, a higher prevalence of intestinal helminths was found in tuberculosis patients compared to the uninfected subjects [31]. Taghipour and colleagues also determined that immunocompromised T.B. patients are more vulnerable to parasitic gastrointestinal infections [32]. It was reported that Blastocystis subtype 1 was the most common subtype found in T.B. patients; however, a phylogenetic analysis revealed no distinction between Blastocystis isolates from T.B. patients and those from the uninfected [31].
S. mansoni was also a risk factor for T.B. infection, and it altered the clinical presentation and pathogenesis of T.B. in Tanzania [33]. The authors recommended treatment of this parasite using praziquantel in T.B. infection management [33].
A systematic review suggested that health education be implemented to help prevent intestinal helminth infection. It further added that screening for helminths should be possibly included in the treatment strategies for tuberculosis patients [31]. Another review suggested an association between Toxoplasma gondii (T. gondii) seropositivity and having tuberculosis, with T. gondii seropositivity, which indicates chronic infection, being relatively common among tuberculosis patients [34].
Strongyloides stercoralis coinfection with pulmonary T.B. was implicated in the cause of the skewed immune response to mycobacterial disease [35]. The proinflammatory Th1 cytokines were reduced, whereas the anti-inflammatory Th2 and Th3 cytokines were elevated, thus leading to a conclusion that helminth coinfection may modulate protective immune responses in latent T.B. [35]. A study of immunological correlates in T.B. coinfection with S. mansoni in Kenya, on the other hand, discovered that the expression of T.B.-specific Th1 cytokines was maintained. Individuals with latent tuberculosis and S. mansoni infection had more CD4+ Th1 cells than those who were only latently T.B.-infected [22]. There were similar results in a Brazilian study, whose findings revealed that A. lumbricoides infection had no impact on Th1, Th2 and Th17 responses or the T cell populations [21].
A Th1 immune response observed during persistent filarial infection was characterized by a reduction in Purified Protein Derivative (PPD)-specific IFN-γ and IL17 responses [36]. The study suggested that filaria infection reduced the PPD-specific IFNγ and IL17 responses. In addition, it was observed that onchocerciasis patients’ peripheral T cells had a weak response to Mtb antigens [37]. Elias and colleagues illustrated that compared to dewormed patients, helminth-infected individuals displayed low Th1 immune response and IFN-γ production in response to mycobacteria infection [38]. Lastly, it has been suggested that a robust Th1 response characterizes cell mediated protection against T.B. infection, and coinfection with helminths could modulate these immune responses by driving Th2 and Treg cells [17][39].
Furthermore, enhanced Treg function is associated with helminth infection and may suppress Th1 responses against unrelated antigens [12][39]. This finding was supported by studies which showed that intestinal helminth coinfection was associated with a reduced Th1 response in active T.B. [16][40]. Type I immunity and their proinflammatory cytokines such as IFN-γ, IL-12 and TNF-α have a protective role against Mtb. By contrast, the induction of type 2 immunity, e.g., Th2 and Treg cells (as seen in helminth infections) and their anti-inflammatory cytokines, were reported to suppress the efficient immune response against T.B. [41].
A mouse model study of Schistosoma mansoni showed a reduced protective efficacy of BCG vaccination against Mtb [38]. Another study demonstrated that concomitant helminth infections significantly impair the immunogenicity of BCG vaccines, an impairment associated with increased TGF-β production [24]. During active T.B., asymptomatic helminth infection has been shown to have a considerable impact on host immunity in a double-blind, randomized clinical study [17]. In comparison to the placebo group, eosinophils and IL-10 levels decreased after albendazole treatment [17]. Another albendazole treatment study was conducted to determine the immunological effects of deworming on proinflammatory cytokine responses to plasmodial antigens. The study demonstrated improvements in immune hypo responsiveness, where anthelmintic treatment significantly increased proinflammatory cytokine responses to Plasmodium falciparum-infected red blood cells [42].
In Egypt, it was determined that hookworm infection was one of the risk factors for the failure of T.B. therapy [43]. However, a human study in the United Kingdom (U.K.), where the authors studied migrants from Nepal, found that hookworm infection reduced T.B. growth and may reduce the risk of infection [20]. According to the evidence presented above, some studies demonstrated that helminthiasis has a negative impact on T.B. diseases, while others showed a beneficial effect. Table 1 summarizes some of the studies investigating helminth and T.B. coinfections.
Table 1. Summary of experimental and human studies focusing on helminth and tuberculosis coinfections.
References Study Type, Location and Helminth(s) Study Aim Major Findings
[44] Human study in Kenya.
Wuchereria bancrofti and Schistosoma haematobium		 To investigate whether prenatal immunity to helminths persists in childhood and if it alters the immune response to BCG Compared to patients who had prenatal sensitization 10–14 months after BCG immunization, T cell IFN-γ production was 26-fold higher in infants who were not sensitized to filariae or schistosomes in utero.
[45] Human study in South Africa.
Ascaris lumbricoides and Trichuris trichiura		 To determine total serum IgE before and after tuberculosis therapy T.B. therapy resulted in reduced serum Ascaris-specific IgE levels. Tuberculin induration was found to be inversely related to IgE in patients but not in controls.
[37] Human study in West Cameroon.
Onchocerca volvulus		 To determine total serum IgE before and after tuberculosis therapy T.B. therapy resulted in reduced serum Ascaris-specific IgE levels. Tuberculin induration was found to be inversely related to IgE in patients but not in controls.
[36] Human study in East Ethiopia.
Ascaris lumbricoides, hookworms, Trichuris trichiura, Strongyloides stercoralis, Hymenolepis nana and Taenia spp.		 To investigate the effect of intestinal helminths on the immune response to PPD in naturally immunized or BCG-vaccinated individuals Individuals who received BCG vaccination and were infected with helminths had reduced T cell and PPD skin test responses. Increased T cell proliferation and IFN were associated with improved BCG efficacy following anthelmintic therapy.
[38] An experimental study in Ethiopia.
Schistosoma mansoni		 To investigate whether chronic helminth-infected individuals have reduced efficacy of BCG vaccine compared to uninfected persons Possibly through attenuation of protective immune responses to mycobacterial antigens and/or by polarizing the general immune responses to the Th2 profile, S. mansoni infection reduced the protective efficacy of BCG vaccination against Mtb.
[23] Human study in Ethiopia.
Ascaris lumbricoides, Hookworm, Strongloides stercoralis, Trichuris trichiura, S. mansoni and Enterobius vermicularis		 To study the prevalence of intestinal helminth infections and their association with active T.B. in T.B. patients and healthy household contacts In addition to HIV infection, intestinal helminth infection may be a risk factor for the development of active pulmonary T.B. This discovery could have significant consequences for the control of tuberculosis in helminth-endemic areas around the world.
[24] Human study in Ethiopia.
Trichuris trichiura, Ascaris lumbricoides, hookworms, Taenia spp., Hymenolepis nana and Enterobius vermicularis		 This study tested anti-helminthic medication before BCG vaccination to determine if it could improve BCG vaccination immunogenicity in helminth-infected patients Chronic worm infection reduced BCG immunogenicity in humans. This was linked to increased TGF-β production but not a better Th2 immune response.
[46] Human study in South Africa.
Ascaris lumbricoides and Trichuris trichiura		 To investigate whether helminth infection could affect a child’s ability to generate a proper Th1 immune response, which was defined by a positive tuberculin skin test (TST) Helminth infection/exposure may reduce the immune response to Mtb infection. In younger children, being Ascaris IgE-positive significantly reduced the likelihood of being TST-positive, but this effect faded as they grew older.
[47] Human study in Venezuela.
Ascaris lumbricoides and Trichuris trichiura		 To investigate the effects of parasite infections, malnutrition and plasma cytokine profiles on tuberculin skin test (TST) positivity TST positivity was associated with low plasma Th1 cytokine levels in indigenous Venezuelan children with T.B. contacts and helminth infections.
[19] Animal study in South Africa.
Nippostrongylus brasiliensis (Nb)		 To investigate the impact of acute Nb-induced lung damage and long-term parasite lung conditioning on the host’s ability to control mycobacterial infection The findings show that early stage Nb infection induces a macrophage response that protects against subsequent mycobacterial infection.
[48] Human study in Ethiopia.
Giardia lamblia, Ascaris lumbricoides, Hookworm spp., Strongyloides stercoralis, Trichuris trichuria, Enterobius vermicularis, Taenia spp., Hymenolepis nana, Schistosoma mansoni or trophozoite stage of Entamoeba histolytica.		 To diagnose latent Mtb infection using the tuberculin skin test (TST) and the IFN-γ release assays in helminth infected school children The tuberculin skin test should be used with caution in areas where parasitic intestinal infections are common.
[49] Human study in Uganda.
Hookworm, Trichuris trichiura, Hymenolepis nana, Schistosoma mansoni, Ascaris lumbricoides, Hymenolepis nana and Schistosoma mansoni		 To determine whether coinfections such as helminths, malaria and HIV modulate the immune system and increase susceptibility to latent tuberculosis infection (LTBI), leading to the persistence of the tuberculosis epidemic Concurrent helminth, malaria and HIV infections did not affect cytokine responses profile in individuals with LTBI.
[50] Human study in Ethiopia.
Schistosoma mansoni		 To investigate whether maternal helminth infection affects maternal and neonatal immunological function and T.B. immunity The combination of early secretory antigenic target 6 (ESAT-6) and culture filtrate protein 10 (CFP-10) elicited a significantly lower IFN-γ response in helminth-positive than in helminth-negative participants. Cord blood mononuclear cells’ (CBMCs) IFN-γ response, total IgE and cross-placental transfer of T.B.-specific IgG were all negatively correlated with maternal helminth infection.
[17] Human study in Ethiopia.
Ascaris lumbricoides Hookworm spp.
Strongyloides stercoralis Trichuris trichiura
Hymenolepis nana
Taenia spp.		 To examine the clinical and immunological effects of helminth infection on T.B. Asymptomatic helminth infection had a profound influence on the immunological profile of individuals with T.B. This favored Th2 immune responses such as increased regulatory T cells and IL-5 and IL-10 secreting cells.
[51] Human study in Ethiopia.
Ascaris lumbricoides		 To investigate the clinical and immunological outcomes of patients coinfected with helminths and T.B. after albendazole treatment The decrease in eosinophil counts and IL-10 demonstrated that asymptomatic helminth infection considerably impacts host immunity during tuberculosis and can be efficiently reversed with albendazole treatment. Helminth infection has clinical effects on chronic infectious diseases such as tuberculosis, and these effects should be further explored.
[52] An animal study in the USA.
Schistosoma mansoni		 To investigate whether Mtb-specific T cell responses can be reversibly impaired by treatment of S. mansoni coinfection, without impacting arginase-1-expressing macrophage-mediated T.B. control Anthelminthic treatment improved Mtb-specific T cell responses. In T.B.-infected mice, arginase-1-expressing macrophages in the lung formed granulomas and exacerbated inflammation.
[53] An experimental animal study in USA.
Heligmosomoides polygyrus		 To investigate whether Mtb infection would be modulated in mice with chronic H. polygyrus infection Despite a systemic increase in FoxP3+ T regulatory cells, neither primary nor memory immunity conferred by Mycobacterium bovis BCG vaccination were affected in mice with chronic enteric helminth infection.
[54] Human study in India.
Strongyloides stercoralis		 To investigate whether helminth modulation of cytokine responses in latent T.B. coinfection is reversible after anthelminthic therapy In Strongyloides stercoralis-latent T.B. coinfection, anthelmintic therapy reversed the modulation of systematic and T.B. antigen-stimulated cytokine responses.
Although HIV is not covered herein, there is evidence of a concurrent distribution of triple disease burden involving tuberculosis, helminths and HIV, particularly in Sub-Saharan Africa. This necessitates a greater focus on disease management strategies by various policymakers [55].

3. Effect of Helminth Infection on T.B. Vaccine

BCG is currently the only T.B. vaccine available; it celebrated its 100th anniversary in 2021. Alternative vaccines are being developed [56]. The BCG vaccine is still the only option for protection against human T.B., and it is inexpensive, safe and widely available. BCG effectiveness against T.B., however, varies in the high helminth-burden areas of the world [56]. Children are typically given the BCG vaccine. A review reported that BCG could provide protection against severe forms of T.B., including meningitis and miliary [57].
The BCG vaccine is administered to more than 80% of all newborns and babies in countries where it is included in the national childhood immunization program; however, it does not prevent the development of latent tuberculosis or the reactivation of pulmonary disease in adults [58]. BCG has been reported to be less effective in T.B.-coinfected individuals living in helminth-endemic areas [36]. However, another study reported no difference in BCG vaccination status and tuberculin skin testing (TST) responses in patients with or without T.B. and helminth coinfection [39].
An Ethiopian study found that helminth infection influenced BCG vaccination outcomes, and PPD-specific cellular immune responses improved in helminth-treated individuals compared to untreated controls [36]. Deworming was shown to boost the efficacy of BCG immunization in this randomized experiment [36]. In addition, it was found that the BCG vaccination of PPD-negative individuals in a helminth-infected population in Ethiopia had poor immunogenicity, and they concluded that this was due to a high Th2 bias in immunological responses caused by chronic helminth infection [36].
Furthermore, in another study, S. mansoni was found to reduce the protective efficacy of BCG vaccination against Mtb, possibly by attenuating protective immune responses to mycobacterial antigens and polarizing general immune responses to a Th2 profile [38].
Th2-like IL-10 responses elicited by intestinal helminths may interfere with Th1-like IFN responses induced by BCG, altering the protective immune response to BCG vaccination [59]. The impact of helminth infection is due to the antigen-specific modification of cell-mediated immunity, and the diminished efficacy could be owing to impaired immune responses to recall antigens [60].
Furthermore, helminth infection during pregnancy has been shown to persist into childhood and shift immunity away from Th1 responses, which are required in T.B. infection and vaccination [44]. Chronic helminth infections increase susceptibility to T.B. infections requiring Th1 responses and also lead to impaired efficacy of the BCG vaccine [24][61].
While there is mounting evidence that helminth prophylaxis could have a role in combating the HIV/AIDS and T.B. pandemics [62], observational research and randomized controlled trials have not revealed a uniform clinical picture. Deworming programs may help to enhance community-based health measures such as proper sanitation, access to clean water and adequate education [63]. More intervention research is required to demonstrate the impact of deworming on tuberculosis disease progression.

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Subjects: Health Care Sciences & Services
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Khethiwe Nomcebo Bhengu
,
Pragalathan Naidoo
,
Ravesh Singh
,
Miranda N. Mpaka-Mbatha
,
Nomzamo Nembe
,
Zamathombeni Duma
,
Roxanne Pillay
,
Zilungile L. Mkhize-Kwitshana
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Update Date: 17 Nov 2022
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