Helminth Parasites Alter Protection against Plasmodium Infection

Table 3

Human studies of coinfection. ARF: acute renal failure, MSM: moderately severe malaria, S: Schistosoma, A: Ascaris, and T: Trichuris.

(a)

Study area	Age of group	Sample (size)	Study design	Helminth type	Outcome for malaria diseases in coinfection	Ref.
Senegal; (Niakhar)	Children	178	Over a 2-year; followup period	S. haematobium	Children with a light S. haematobium infection presented lower P. falciparum parasite densities than children not infected by S. haematobium	[112]
Mali; (Tieneguebougou and Bougoudiana)	Children and young adults	62	Followed prospectively through a malaria; transmission season	Wuchereria bancrofti; Mansonella perstans	Pre-existent filarial infection attenuates immune responses associated with severe malaria and protects against anemia, but has little effect on susceptibility to or severity of acute malaria infection	[113]
Southern; Ethiopia	1 to 82 years; Mean; 18.6 years	1,065 febrile patients	Cross-sectional	A. lumbricoides; T.trichiura, S. mansoni, and hookworm	The chance of developing non-severe malaria were 2.6–3.3 times higher in individuals infected with helminth, compared to intestinal helminth-free individuals; The odds ratio for being infected with non-severe P. falciparum increased with the number of intestinal helminth species	[114]
South-central; Côte d’Ivoire	Infants; (6–23 months),; children; (6–8 year), and young women; (15–25 years)	732 subjects	Cross-sectional survey	Soil-transmitted helminth	Coinfected children had lower odds of anemia and iron deficiency.; Interaction between P. falciparum and light-intensity hookworm infections vary with age.	[115]
Brasil (Careiro)	School children; 5 to 14 years	236	Cohort and cross-sectional	A. lumbricoides; hookworm and T. trichiura	Helminthes protect against hemoglobin decrease during an acute malarial attack by Plasmodium.	[116]
Thailand; (Bangkok)	Mean 24 years (range; 15–62)	537 files	Retrospective case-control	A. lumbricoides	Percentage protection for mild controls against cerebral malaria ranged from 40% for Ascaris (present/absent) to 70% for Ascaris medium infection. For intermediate controls protection against cerebral malaria was 75% for Ascaris (present/absent).	[117]
Thailand; (Bangkok)	19–37 years; 22 patients with malaria-associated ARF and 157 patients with MSM	179	Retrospective case-control	A. lumbricoides, T. trichiura, hookworm, and Strongyloides; stercoralis	Helminths were associated with protection from renal failure; Helminth-infected controls were less likely to have jaundice or to have peripheral mature schizonts than controls without helminths	[118]

(b)

Study area	Age of group	Sample (size)	Study design	Helminth type	Outcome for malaria diseases in coinfection	Ref.
Kenya (Kingwede)	8 years and older	561	cross-sectional	S. haematobium	Children had 9.3 times the odds of coinfection; compared to adults	[119]
Nigeria; (Osun)	preschool children; (6–59 months)	690	Double-blind and randomized	A. lumbricoides	There was no significant difference in the severity of anaemia.	[120]
Kabale,; Uganda	All ages (856)	856	Retrospective; 18 months	A. lumbricoides, T. trichiura, and hookworm	Non evidence for an association and risk of malaria	[121]

(c)

Study area	Age of group	Sample (size)	Study design	Helminth type	Outcome for malaria diseases in coinfection	Ref.
Senegal (Niakhar and Bambey)	Children, mean 6.6 years	105	Prospective case-control	A. lumbricoides	Prevalence of A. lumbricoides infection was higher in cases of severe malaria	[123]
Northern; Senegal	Children aged 6–15 years	512	Cohort	S. mansoni	The incidence rate of malaria attacks was higher among S. mansoni-infected individuals carrying the highest worm loads. In contrast, the rate of malaria attacks were lower in medium grade S. mansoni infections	[124]
Ghana; (Kumasi)	Women; (15–48 years); mean 26.8 years	746	Cross-sectional	A. lumbricoides, T. trichiura, S. stercoralis, and E. vermicularis	Coinfection resulted in increased risks of anemia, low birth weight, and small for gestational age infants	[125]
Ethiopia; (Alaba Kulito)	Children <5 years, children 5–14 years, and adults ≥15 years	1802 acute febrile patients	case-control	Hookworm,; A. lumbricoides, and T. trichiura	Coinfection is associated with higher anaemia prevalence and low weight status than single infection with Plasmodium in children	[126]
Kenya; (Makueni)	Primary school children; 4–17 years	(221 and 228)	Cross-sectional	S. mansoni	Hepatosplenomegaly due to proinflammatory mechanism exacerbated by schistosomiasis	[127]
Kenya (Mangalete)	Children; 4–17 years	79	Cross-sectional	S. mansoni	Hepatosplenomegaly is associated with low regulatory and Th2 response to Schistosome antigens	[128]
Zimbabwe (Burma Valley)	Children 6–17 years	605	12-month followup of a cohort of children	Schistosome	Increased prevalence of malaria parasites and had higher sexual stage malaria parasite in children coinfected with schistosomiasis	[129]
Cameroon; (Bolifamba)	9 months to 14 years	425 children		A. lumbricoides,; T. trichiura, and hookworm	Coinfections in which heavy helminth loads showed high P. falciparum parasite loads compared with coinfections involving light helminth burden	[130]