Table 4.
Associations Between Helminth Infection and Metabolic Outcomes
| Helminth and Metabolic Outcome | Mean | Crude Mean Difference (95% CI)a | P Value | Adjusted Mean Difference (95% CI)b | P Value |
|---|---|---|---|---|---|
| HOMA-IR | |||||
| Schistosoma mansoni, stool Kato-Katz | |||||
| Uninfected (n = 1065) | GM, 1.90 | … | … | ||
| Infected (n = 440) | GM, 1.69 | −0.05 (−.12 to .02) | .12 | 0.05 (−.05 to .15) | .28 |
| S. mansoni, stool PCR | |||||
| Uninfected (n = 793) | GM, 1.62 | … | … | ||
| Infected (n = 694) | GM, 2.06 | −0.10 (−.21 to .01) | .07 | −0.01 (−.08 to .06) | .77 |
| S. mansoni intensity, stool Kato-Katz | |||||
| Uninfected (n = 1065) | GM, 1.90 | … | … | ||
| Light (n = 230) | GM, 2.07 | 0.04 (−.09 to .17) | 0.09 (−.07 to .25) | ||
| Moderate (n = 121) | GM, 1.20 | −0.20 (−.35 to −.05) | −0.04 (−.19 to .12) | ||
| Heavy (n = 89) | GM, 1.61 | −0.07 (−.21 to .06) | .07 | 0.07 (−.11 to .25) | .69 |
| Trichuris trichiura, stool Kato-Katz | |||||
| Uninfected (n = 1383) | GM, 1.82 | … | … | ||
| Infected (n = 122) | GM, 2.00 | 0.04 (−.08 to .17) | .50 | 0.08 (−.05 to .20) | .21 |
| Hookworm, stool PCR | |||||
| Uninfected (n = 1309) | GM, 1.83 | … | … | ||
| Infected (n = 55) | GM, 1.76 | −0.02 (−.17 to .14) | .83 | 0.11 (−.18 to .40) | .45 |
| Strongyloides stercoralis stool PCR | |||||
| Uninfected (n = 1385) | GM, 1.89 | … | … | ||
| Infected (n = 101) | GM, 1.25 | −0.18 (−.40 to .035) | .10 | 0.04 (−.16 to .24) | .70 |
| Infection with multiple helminth species (S. mansoni [PCR], T. trichiura, hookworm, and S. stercoralis) | |||||
| Helminth uninfected (n = 655) | GM, 2.12 | … | … | ||
| Infected with any 1 helminth (n = 611) | GM, 1.58 | −0.13 (−.23 to −.03) | −0.04 (−.12 to .04) | ||
| Infected with any 2 helminths (n = 155) | GM, 1.90 | −0.05 (−.18 to .09) | 0.13 (.03–.23) | ||
| Infected with any 3 or 4 helminths (n = 17) | GM, 1.11 | −0.28 (−.58 to .02) | <.01 | −0.22 (−.66 to .23) | .05 |
| Infection with multiple helminth species (test for trend) | … | −0.07 (−.12 to −.02) | .01 | 0.01 (−.04 to .06) | .61 |
| Triglycerides (mmol/L) | |||||
| S. mansoni, stool Kato-Katz | |||||
| Uninfected (n = 1065) | GM, 1.02 | … | … | ||
| Infected (n = 440) | GM, 0.90 | −0.05 (−.12 to .01) | .12 | −0.05 (−.14 to .03) | .21 |
| S. mansoni, stool PCR | |||||
| Uninfected (n = 793) | GM, 1.00 | … | … | ||
| Infected (n = 694) | GM, 0.95 | −0.02 (−.07 to .02) | .28 | −0.04 (−.08 to .01) | .09 |
| S. mansoni intensity, stool Kato-Katz | |||||
| Uninfected (n = 1065) | GM, 1.02 | … | … | ||
| Light (n = 230) | GM, 0.95 | −0.03 (−.15 to .08) | −0.05 (−.18 to .08) | ||
| Moderate (n = 121) | GM, 0.98 | −0.02 (−.11 to .08) | 0.00 (−.09 to .09) | ||
| Heavy (n = 89) | GM, 0.72 | −0.15 (−.23 to −.08) | <.01 | −0.13 (−.20 to 0.07) | <.01 |
| T. trichiura, stool Kato-Katz | |||||
| Uninfected (n = 1383) | GM, 0.99 | … | … | ||
| Infected (n = 122) | GM, 0.87 | −0.06 (−.11 to −.00) | .04 | −0.05 (−.13 to .04) | .29 |
| Hookworm, stool PCR | |||||
| Uninfected (n = 1309) | GM, 0.97 | … | … | ||
| Infected (n = 55) | GM, 0.67 | −0.17 (−.30 to −.03) | .02 | −0.08 (−.25 to .09) | .32 |
| S. stercoralis, stool PCR | |||||
| Uninfected (n = 1385) | GM, 0.97 | … | … | ||
| Infected (n = 101) | GM, 0.95 | −0.01 (−.09 to .08) | .84 | −0.05 (−.15 to .05) | .32 |
| Infection with multiple helminth species (S. mansoni [PCR], T. trichiura, hookworm, and S. stercoralis) | |||||
| Helminth uninfected (n = 655) | GM, 0.99 | … | … | ||
| Infected with any 1 helminth (n = 611) | GM, 0.97 | −0.01 (−.04 to .03) | −0.01 (−.05 to .02) | ||
| Infected with any 2 helminths (n = 155) | GM, 0.87 | −0.05 (−.12 to .01) | −0.07 (−.15 to .02) | ||
| Infected with any 3 or 4 helminths (n = 17) | GM, 0.65 | −0.18 (−.37 to .01) | .23 | −0.20 (−.49 to .09) | .50 |
| Infection with multiple helminth species (test for trend) | … | −0.03 (−.05 to .00) | .06 | −0.03 (−.07 to .01) | .12 |
| Total cholesterol (mmol/L) | |||||
| S. mansoni, stool Kato-Katz | |||||
| Uninfected (n = 1065) | 4.64 | … | … | ||
| Infected (n = 440) | 4.24 | −0.40 (−.62 to −.19) | <.01 | −0.25 (−.44 to −.07) | .01 |
| S. mansoni, stool PCR | |||||
| Uninfected (n = 793) | 4.69 | … | … | ||
| Infected (n = 694) | 4.32 | −0.37 (−.63 to −.11) | .007 | −0.28 (−.53 to −.03) | .03 |
| S. mansoni intensity, stool Kato-Katz | |||||
| Uninfected (n = 1065) | 4.64 | … | … | ||
| Light (n = 230) | 4.34 | −0.30 (−.54 to −.07) | −0.19 (−.42 to .05) | ||
| Moderate (n = 121) | 4.17 | −0.48 (−.77 to −.19) | −0.33 (−.59 to −.08) | ||
| Heavy (n = 89) | 4.10 | −0.55 (−.87 to −.23) | .01 | −0.33 (−.62 to −.04) | .06 |
| T. trichiura, stool Kato-Katz | |||||
| Uninfected (n = 1383) | 4.53 | … | … | ||
| Infected (n = 122) | 4.39 | −0.14 (−.42 to .15) | .33 | 0.00 (−.25 to .24) | .99 |
| Hookworm, stool PCR | |||||
| Uninfected (n = 1309) | 4.53 | … | … | ||
| Infected (n = 55) | 4.06 | −0.47 (−.76 to −.18) | .003 | −0.22 (−.53 to .09) | .16 |
| S. stercoralis, stool PCR | |||||
| Uninfected (n = 1385) | 4.53 | … | … | ||
| Infected (n = 101) | 4.24 | −0.29 (−.61 to .03) | .07 | −0.22 (−.53 to .08) | .15 |
| Infection with multiple helminth species (S. mansoni [PCR], T. trichiura, hookworm, and S. stercoralis) | |||||
| Helminth uninfected (n = 655) | 4.71 | … | … | ||
| Infected with any 1 helminth (n = 611) | 4.37 | −0.34 (−.62 to −.06) | −0.27 (−.53 to −.01) | ||
| Infected with any 2 helminths (n = 155) | 4.23 | −0.48 (−.83 to −.13) | −0.32 (−.63 to −.01) | ||
| Infected with any 3 or 4 helminths (n = 17) | 3.75 | −0.97 (−1.49 to −.44) | .01 | −0.53 (−1.08 to .02) | .11 |
| Infection with multiple helminth species (test for trend) | … | −0.29 (−.48 to −.09) | <.01 | −0.20 (−.36 to −.03) | .02 |
| LDL-c (mmol/L) | |||||
| S. mansoni, stool Kato-Katz | |||||
| Uninfected (n = 1065) | 2.80 | … | … | ||
| Infected (n = 440) | 2.37 | −0.43 (−.74 to −.12) | .01 | −0.25 (−.49 to −.02) | .04 |
| S. mansoni, stool PCR | |||||
| Uninfected (n = 793) | 2.87 | … | … | ||
| Infected (n = 694) | 2.45 | −0.42 (−.78 to −.05) | .03 | −0.28 (−.57 to .01) | .06 |
| S. mansoni intensity, stool Kato-Katz | |||||
| Uninfected (n = 1065) | 2.80 | … | … | ||
| Light (n = 230) | 2.49 | −0.32 (−.60 to −.03) | −0.23 (−.46 to .00) | ||
| Moderate (n = 121) | 2.18 | −0.62 (−.97 to −.28) | −0.39 (−.72 to −.05) | ||
| Heavy (n = 89) | 2.34 | −0.46 (−.91 to −.01) | <.01 | −0.14 (−.51 to .23) | .04 |
| T. trichiura, stool Kato-Katz | |||||
| Uninfected (n = 1383) | 2.66 | … | … | ||
| Infected (n = 122) | 2.69 | 0.03 (−.32 to .37) | .87 | 0.05 (−.22 to .33) | .7 |
| Hookworm, stool PCR | |||||
| Uninfected (n = 1309) | 2.67 | … | … | ||
| Infected (n = 55) | 2.13 | −0.55 (−.79 to −.30) | <.01 | 0.08 (−.19 to .35) | .55 |
| S. stercoralis, stool PCR | |||||
| Uninfected (n = 1385) | 2.69 | … | … | ||
| Infected (n = 101) | 2.34 | −0.35 (−.58 to −.12) | .004 | −0.32 (−.53 to −.12) | .003 |
| Infection with multiple helminth species (S. mansoni [PCR], T. trichiura, hookworm, and S. stercoralis) | |||||
| Helminth uninfected (n = 655) | 2.90 | … | … | ||
| Infected with any 1 helminth (n = 611) | 2.48 | −0.42 (−.82 to −.02) | −0.27 (−.55 to .02) | ||
| Infected with any 2 helminths (n = 155) | 2.44 | −0.46 (−.78 to −.13) | −0.29 (−.54 to −.05) | ||
| Infected with any 3 or 4 helminths (n = 17) | 1.96 | −0.94 (−1.57 to −.31) | .02 | −0.52 (−1.14 to .10) | .10 |
| Infection with multiple helminth species (test for trend) | … | −0.30 (−.53 to −.07) | .01 | −0.19 (−.35 to −.04) | .02 |
| HDL-c (mmol/L) | |||||
| S. mansoni, stool Kato-Katz | |||||
| Uninfected (n = 1065) | GM, 1.81 | … | … | ||
| Infected (n = 440) | GM, 1.82 | 0.09 (−.14 to .14) | .98 | 0.05 (−.04 to .14) | .26 |
| S. mansoni, stool PCR | |||||
| Uninfected (n = 793) | GM, 1.83 | … | … | ||
| Infected (n = 694) | GM, 1.79 | −0.01 (−.16 to .14) | .92 | 0.00 (−.09 to .09) | .96 |
| S. mansoni intensity, stool Kato-Katz | |||||
| Uninfected (n = 1065) | GM, 1.81 | … | … | ||
| Light (n = 230) | GM, 1.80 | −0.01 (−.10 to .09) | 0.06 (−.03 to .14) | ||
| Moderate (n = 121) | GM, 2.19 | 0.08 (−.08 to .24) | 0.12 (−.01 to .26) | ||
| Heavy (n = 89) | GM, 1.49 | −0.08 (−.34 to .17) | .02 | −0.07 (−.22 to .09) | .07 |
| T. trichiura, stool Kato-Katz | |||||
| Uninfected (n = 1383) | GM, 1.83 | … | … | ||
| Infected (n = 122) | GM, 1.62 | −0.06 (−.18 to .07) | .38 | 0.00 (−.12 to .12) | .97 |
| Hookworm, stool PCR | |||||
| Uninfected (n = 1309) | GM, 1.84 | … | … | ||
| Infected (n = 55) | GM, 2.02 | 0.04 (−.18 to .26) | .70 | −0.03 (−.13 to .08) | .57 |
| S. stercoralis, stool PCR | |||||
| Uninfected (n = 1385) | GM, 1.81 | … | … | ||
| Infected (n = 101) | GM, 1.79 | −0.01 (−.10 to .09) | .92 | −0.04 (−.13 to .05) | .36 |
| Infection with multiple helminth species (S. mansoni [PCR], T. trichiura, hookworm, and S. stercoralis) | |||||
| Helminth uninfected (n = 655) | GM, 1.82 | … | … | ||
| Infected with any 1 helminth (n = 611) | GM, 1.83 | 0.00 (−.16 to .17) | 0.00 (−.10 to .10) | ||
| Infected with any 2 helminths (n = 155) | GM, 1.70 | −0.03 (−.16 to .11) | −0.02 (−.11 to .07) | ||
| Infected with any 3 or 4 helminths (n = 17) | GM, 1.75 | −0.02 (−.24 to .21) | .86 | 0.05 (−.19 to .28) | .89 |
| Infection with multiple helminth species (test for trend) | … | −0.01 (−.10 to .09) | .88 | −0.00 (−.06 to .05) | .89 |
| Diastolic BP (mm Hg) | |||||
| S. mansoni, stool Kato-Katz | |||||
| Uninfected (n = 1065) | 76.30 | … | … | ||
| Infected (n = 440) | 75.86 | −0.44 (−1.89 to 1.01) | .54 | 0.72 (−1.40 to 2.84) | .49 |
| S. mansoni, stool PCR | |||||
| Uninfected (n = 793) | 76.35 | … | … | ||
| Infected (n = 694) | 75.88 | −0.46 (−1.48 to .56) | .36 | 0.56 (−.84 to 1.95) | .42 |
| S. mansoni intensity, stool Kato-Katz | |||||
| Uninfected (n = 1065) | 76.30 | … | … | ||
| Light (n = 230) | 76.58 | 0.27 (−1.08 to 1.63) | 1.25 (−.71 to 3.22) | ||
| Moderate (n = 121) | 76.75 | 0.45 (−2.56 to 3.47) | 1.55 (−2.35 to 5.46) | ||
| Heavy (n = 89) | 72.84 | −3.46 (−4.81 to −2.12) | <.01 | −2.29 (−3.91 to −.68) | .01 |
| T. trichiura, stool Kato-Katz | |||||
| Uninfected (n = 1383) | 76.40 | … | … | ||
| Infected (n = 122) | 72.97 | −3.43 (−5.64 to −1.22) | <.01 | −1.45 (−3.58 to .69) | .18 |
| Hookworm, stool PCR | |||||
| Uninfected (n = 1309) | 76.35 | … | … | ||
| Infected (n = 55) | 72.44 | −3.90 (−7.22 to −.59) | .02 | 2.20 (−.92 to 5.33) | .16 |
| S. stercoralis, stool PCR | |||||
| Uninfected (n = 1385) | 76.09 | … | … | ||
| Infected (n = 101) | 76.60 | 0.51 (−2.67 to 3.69) | .74 | −0.56 (−3.25 to 2.14) | .68 |
| Infection with multiple helminth species (S. mansoni [PCR], T. trichiura, hookworm, and S. stercoralis) | |||||
| Helminth uninfected (n = 655) | 76.44 | … | … | ||
| Infected with any 1 helminth (n = 611) | 76.34 | −0.10 (−1.22 to 1.02) | 0.87 (−.80 to 2.53) | ||
| Infected with any 2 helminths (n = 155) | 74.07 | −2.37 (−4.33 to −.41) | 0.08 (−2.21 to 2.38) | ||
| Infected with any 3 or 4 helminths (n = 17) | 70.78 | −5.66 (−12.24 to .91) | .10 | −4.11 (−10.33 to 2.11) | .47 |
| Infection with multiple helminth species (test for trend) | … | −0.94 (−1.70 to −.18) | .02 | −0.26 (−1.13 to .61) | .54 |
Abbreviations: BP, blood pressure; CI, confidence interval; GM, geometric mean; HDL-c, high-density lipoprotein cholesterol; HOMA-IR, homeostatic model assessment of insulin resistance; LDL-c, low-density lipoprotein cholesterol; PCR, polymerase chain reaction.
aBoth crude and adjusted results allowed for the survey design—that is, weighting and clustering.
bAdjusted for the following variables: HOMA-IR (age, sex, occupation, residence, lake contact, treatment for worms, treatment with coartem, body mass index [BMI], family history of diabetes mellitus, maternal and paternal tribe); triglycerides (age, sex, occupation, residence, diet, treatment for worms, family history of obesity, paternal and maternal tribe); total cholesterol (age, sex, occupation, residence, diet, exercise, family history of obesity, paternal and maternal tribe); LDL-c (age, sex, occupation, diet, exercise, treatment for worms, treatment with coartem, parental tribe); HDL-c (age, sex, occupation, residence, diet, treatment for worms, treatment with coartem, parental tribe); diastolic BP (age, sex, occupation, residence, lake contact, treatment for worms, paternal tribe, BMI). There was no evidence of association between helminth infection and fasting blood glucose, glycated hemoglobin, systolic BP, BMI, waist circumference, or waist-to-hip ratio (see Supplementary Table 2).