Table 1.

Summary of articles investigating associations between helminths and allergy‐related diseases outcomes in Africa from January 2008 to March 2018

Article	Sample size (N) & Study design	Age (years)	Country & Setting	Worm burden (%)	Allergy‐related outcomes	Effect size [OR/HR (CI), P‐value]
Hartgers, et al24	123 Cross‐sectional	5‐14	Ghana Rural	Any helminth—52% S. haematobium—38% Hookworm—24%	SPT in S. haematobium uninfected —19%, SPT in S. haematobium infected —11%	S. haematobium ↔SPT 0.26 (0.07‐1.00), P = 0.05
Calvert, and Burney, 11	773 Case‐control	8‐12	South Africa Rural & Urban	Ascaris—61% T. trichiura—33%	EIB in rural—8.7% EIB in urban—14.9% SPT with EIB —20.7% SPT without EIB —3.7%	Ascaris ↔EIB 1.87 (1.19‐2.95), P = 0.009 T. trichiura ↔EIB 0.99 (0.74‐1.35), P = 0.99 Ascaris ↔SPT 0.63 (0.42‐0.94), P = 0.03
Amberbir, et al25	878 Cross‐sectional	3	Ethiopia Rural & Urban	Hookworm—4.9% A. lumbricoides—4.3% Any geo‐helminths—8.5%	Wheeze—9% Eczema—6.3% Hay fever—5% Any SPT—8.7%	Any geo‐helminths ↔ Wheeze [0.74 (0.29‐1.90), P = 0.53] Eczema [0.39 (0.09‐1.63), P = 0.19] Hay fever [0.49 (0.12‐2.09), P = 0.33] SPT [1.25 (0.57‐2.73), P = 0.58]
Ige, et al26	110 Case‐control	Adults, mean = 38	Nigeria Rural & Urban	Taenia solium—11% (asthmatics) vs 13% (controls) A. lumbricoides—11% (asthmatics) vs 9% (controls)	55 asthmatics & 55 controls	Not significant (values not reported)
Larbi, et al27	1482 Cross‐sectional	6‐15	Ghana Rural & Urban	S. haematobium—2.7% urban, 10% rural Hookworm—2% urban, 12% rural Ascaris spp—0% urban, 14.5% rural Trichuris spp—0.3% urban, 2.5% rural	SPT in urban—17.8% SPT in rural—25%	Single helminths – Not significant
Mpairwe, et al28	2507 RCTa	0‐1	Uganda Peri‐urban	Mother's worms in pregnancy: Hookworm—44% S. mansoni—18.3%	Eczema in first year of life—rate 10.4/100 PYFU Reported recurrent wheeze at 1 y—9%	Albendazole in pregnancy→eczema (physician‐diagnosed, 0‐1 y) 1.82 (1.26‐2.64), P = 0.002 Praziquantel in pregnancy (if mother had S. mansoni) →eczema (physician‐diagnosed 0‐1 y) 2.65 (1.16‐6.08), not significant if mother had no S. mansoni; interaction P = 0.02. Albendazole in pregnancy→reported wheeze (at 1 y) 1.58 (1.13‐2.22), P = 0.008
Smedt, et al29	3041 Cross‐sectional	7‐14	Rwanda Rural & Urban	Any of 10 helminth species (eggs) in stool—23.1%	Vernal Keratoconjunctivitis—4%	Any helminths↔vernal keratoconjunctivitis 1.0 (0.6‐1.7), P = 0.95
Stevens, et al30	198 Case‐control	6‐16	Ghana Rural & Urban	Only 4 had any helminths	99 asthmatics & 99 controls	Not significant (values not reported)
Rujeni, et al31	672 Cross‐sectional	1‐86	Zimbabwe Rural	S. haematobium—52.9% & 8.6% in high & low transmission areas	SPT—17.7%	SPT size inversely related to S. haematobium intensity, in high transmission area only r = ‐0.101, P = 0.037
Amare, et al32	405 Cross‐sectional	Mean 12.09 ± 2.54	Ethiopia Town	Any helminth—22.7%, A. lumbricoides—48%, Hymenolepis nana—28%, Hookworm—9%, T. trichiura—6.6%	History of any reported allergy—8%	Associations between helminths reported as not significant (actual numbers not shown)
Amoah, et al33	1604 Cross‐sectional	5‐16	Ghana Rural & Urban	Any intestinal helminths—18% S. haematobium—7%	Adverse reactions to peanuts—1.5% Peanut SPT—2%	Any intestinal helminths ↔reported adverse reactions to peanut 0.35 (0.08‐1.56), P = 0.17 Any intestinal helminths ↔peanut SPT 0.69 (0.17‐2.84), P = 0.61 S. haematobium ↔ reported adverse reactions to peanut 0.65 (0.08‐4.95), P = 0.67 S. haematobium ↔peanut SPT 0.41 (0.05‐3.42), P = 0.41
Oluwole, et al34	170 Case‐control	13‐14	Nigeria Rural & Urban	A. lumbricoides—17% asthmatics, 13% controls Hookworm—5% asthmatics, 4% controls	SPT—73% asthmatics, 60% controls	No statistically significant associations reported (actual values not shown)
Mpairwe, et al35	2507 pregnant women, 2345 live births Birth cohortb	0‐5	Uganda Peri‐urban	Mother's helminths in pregnancy: Hookworm—45%, Mansonella perstans—21%, S. mansoni—18%, Strongyloides stercoralis—12%, T. trichiura—9% Children's worms in first 5 y: T. trichiura—21%, A. lumbricoides—11%, S. mansoni—7%, Hookworm—6%	Doctor‐diagnosed eczema‐rate in first 5 y—4.68/100 PYFU	Mother's hookworm→eczema 0‐5 y 0.71 (0.51‐0.99), P = 0.04 Mother's hookworm modified effects on other known eczema risk factors Mother's other helminths ‐not significant Childhood T. trichiura ↔eczema 0‐5 y 0.35 (0.18‐0.67), P = 0.002 Childhood hookworm ↔eczema 0‐5 y 0.33 (0.11‐1.02), P = 0.05 Other childhood helminths‐not significant
Obeng, et al36	1385 Cross‐sectional	5‐16	Ghana Rural & Urban	Hookworm—9.9% Schistosoma spp—9.5% Ascaris spp—6.2% Trichuris spp—1.9% Any helminths—23.1%	Reported asthma—8.2% Wheeze—7.9% Any SPT—18%	For wheeze and asthma, no significant associations were seen with single or combined helminth infections Schistosoma spp ↔mite SPT 0.15 (0.05‐0.41), P < 0.0001 Schistosoma spp ↔cockroach SPT 0.49 (0.18‐1.29), P = 0.15 Trichuris spp ↔cockroach SPT 3.73 (1.22‐11.41), 0.02; but no association with mite SPT No significant association between all other helminths and SPT
Pinot de Moira, et al37	240 Cross‐sectional	7‐16	Uganda Rural (Fishing village)	S. mansoni—93.8% Hookworm—80.4% Other helminths—37%	Wheeze—8.2% Dust mite SPT—4.2%	Hookworm ↔wheeze 0.29 (0.10‐0.87), P = 0.03 S. mansoni infection intensity ↔wheeze 1.05 (0.82‐1.34) Helminths ↔SPT reported as not significant (data not shown)
Webb, et al38	2316 Cross‐sectional survey	Median 24, IQR 8.32	Uganda Rural (Fishing village islands)	S. mansoni (KK)—51%; (CCA)—72% Hookworm (PCR)—22% S. stercoralis (PCR)—12%; T. trichiura—10%; A. lumbricoides—1.2%	Wheeze <5 y—2% Wheeze ≥5 y—5% Any SPT—19%	A. lumbricoides ↔wheeze 6.36 (1.10‐36.63), P = 0.04 All other helminths—not significantly associated with wheeze T. trichiura ↔SPT 2.08 (1.38‐3.15), P = 0.001 All other helminths—not associated with SPT
Namara, et al39	1188 RCT (& birth cohort)	9	Uganda Peri‐urban	Mother's infection during pregnancy: Hookworm—42.6%, S. mansoni—19.3% Children's infections at 9 y: S. mansoni—11%, T. trichiura—4%, A. lumbricoides—1%	Wheeze—3.7% Doctor‐diagnosed eczema—2.3% Reported eczema—3.4% Doctor‐diagnosed asthma—1.2% Any SPT—25%	Maternal albendazole in pregnancy→wheeze at 9 y—0.70 (0.31‐1.57); SPT at 9 y—0.96 (0.68‐1.37) Maternal praziquantel in pregnancy→wheeze at 9 y—1.53 (0.69‐3.43); SPT—1.13 (0.79‐1.61) Childhood albendazole→wheeze at 9 y—1.01 (0.01 (0.46‐2.23); SPT at age 9 y—1.00 (0.71‐1.43)

OR, odds ratio; HR, hazard ratio; CI, confidence interval; SPT, skin prick test positive for allergic sensitization; EIB, exercise‐induced bronchospasm; RCT, randomized controlled trial; PYFU, person‐years of follow‐up; KK, Kato‐Katz method; CCA, circulating cathodic antigen; PCR, polymerase chain reaction

↔ the two variables tested for association in case‐control or cross‐sectional studies.

→ the two variables tested for association in clinical trial or birth cohort.

^aRCT albendazole vs placebo and praziquantel vs placebo in pregnancy as 2 × 2 factorial design, followed by albendazole vs placebo in childhood 15 months to 5 years.

^bBirth cohort following the RCT above.