Review Article

Helminth Parasites Alter Protection against Plasmodium Infection

Table 4

Helminthic infection drives immune response to challenge with Plasmodium. The time after helminth infection when the Plasmodium challenge was performed. ND: nondetermined, wks: weeks, KO: knockout, ECM: experimental cerebral malaria.
(a)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

ICR HSDP. berghei
ANKA
S. mansoni 7 wksLow rates of ECM (30%), delay in death associated with high levels of IL-4, IL-10[136]
C57BL/6P. berghei
ANKA
S. japonicum 8 wksIncreased survival rate and reduction of the brain pathology. Th2 response induced by worm plays an important role in protecting against ECM[137]
C57BL/6P. berghei
ANKA
S. mansoni 8-9 wksIncreased parasitemia, mortality, weight loss, and hypothermia; decreased pathology in the brain associated with high levels of IL-5, IL-13 and low serum IFN-[138]
Swiss albinoP. berghei
ANKA
S. mansoni 7 wksIncreased parasitemia and mortality
Delayed reduction/elimination of the parasite followed by administration of antimalarial treatment
[139]
C57BL/6P. chabaudiS. mansoni 8 wksIncreased parasitemia associated with a deficiency in the production of TNF-[140]
BALB/cP. yoelii NXL 
(non-lethal)
S. mansoni 2, 4, and 6 wksIncreased parasitemia and death at 6 wks of coinfection. Hepatosplenomegaly was more marked in coinfected mice compared to either disease separately[141]
A/JP. chabaudi S. mansoni 8 wksMice escape death and showed high production of IFN-[142]

(b)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

C57BL/6P. chabaudi H. polygyrus 2, 3, or 5 wksIncreased parasitemia and mortality associated with low levels of IFN-γ and high levels of TGF-, IL-10[143]
C57BL/6P. chabaudi AS H. polygyrus 2 wksIncreased parasitemia; however, it ameliorates severe hypothermia and hypoglycaemia; besides this, it induced earlier reticulocytosis than Pc-infected WT mice[144]
C57BL/6 
IFN/
IL-23/
P. chabaudi AS H. polygyrus At the same timeIncreased mortality and severe liver disease, associated with increased IFN-γ, IL-17, and IL-22 in the liver. The coinfected IFN/ and IL-23/ mice survive[145]
C57BL/6 
BALB/c
P. chabaudi AS H. polygyrus 2 wks 
with AgPc + adjuvant
Suppresses the protective efficacy of the malaria vaccine. Deworming treatment before antimalarial immunization restored the protective immunity to malaria challenge[146]
C57BL/6P. yoelii 17 XNLH. polygyrus 2 wksIncreased pathology due to reduced response against Py (low levels of IFN-γ) in the spleen cells, as a result of higher activation of Treg [147]
BALB/cP. yoelii
17 NXL
H. polygyrus 3 wksReduction of pathology, low levels of IFN-, and high levels of IL-4 induced by helminthes[148]
C57BL/6P. berghei ANKAH. polygyrus 2 wksHp infection did not alter ECM development, despite accelerated P. berghei growth in vivo [149]
C57BL/6 BALB/cP. berghei ANKAH. polygyrus 2 wksNo differences [150]

(c)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

BALB/cP. yoelii 17 NXLE. caproni 3 wksEc showed counterregulatory antiparasite cytokine responses to non-lethal strain PyNXL (less IFN- and high IL-4 levels induced by )[148]
BALB/cP. yoelii 17 NXLE. caproni 5 wks Increased mortality and pathology; the pathology was reversible through clearance of by praziquantel treatment[151]
BALB/c P. yoelii 17XL E. caproni 5 wks does not alter the course of Py17XL infection[151]

(d)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

C57BL/6P. yoelii 17NXL Strongyloides ratti 1 wkDid not altered cytokine response[152]
BALB/cP. berghei ANKAStrongyloides ratti 1 wkThe coinfection did not change the efficacy of vaccination against Pb [153]

(e)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

BALB/cP. chabaudi Nippostrongylus
brasiliensis
Same dayReduction of anemia and parasitemia. Th2 response was inhibited by Plasmodium [154]
C57BL/6P. berghei Nippostrongylus brasiliensis 3 wksDelayed peak parasitemia, increased survival[155]

(f)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

BALB/cP. chabaudi L. sigmodontis 8 wksIncreased severity of the anemia and weight loss associated with increased IFN-[156]
C57BL/6 
IL-10KO
P. berghei
(ANKA)
L. sigmodontis 8 wks Reduction of ECM associated with increased IL-10 
IL-10KO mice coinfected with Pb-Ls die of ECM
[157]
BALB/cP. berghei ANKAL. sigmodontis 2 wksReduced protection against P. berghei challenge infection for low frequencies of CSP-specific CD8 T cells, CSP-specific IFN-γ and TNF-α production [153]

(g)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

CBAP. berghei
(ANKA)
Brugia pahangi
irradiated attenuated
1 wkIncreased survival and protected them against the ECM development; increase synthesis of IFN-, IL-4, IL-5, and IgE[158]

(h)

Background mousePlasmodium strainHelminth typeCoinfection timeMalaria disease outcomeRef.

C57BL/6P. berghei Trichinella spiralis 1–4 wksPartially subdued parasitaemia and prolonged survival[159]