Prevalence of helminths infection
Among 1,065 febrile patients examined for malaria, 702 were volunteered to provide stool samples for the diagnosis of infection with intestinal helminths. There was no significant difference in baseline demographics between those who provided stool sample and those who did not (data not shown). Out of 702 patients examined, 53.8% were positive for at least one intestinal helminth species (Table
2). The diagnosed helminth species were
A. lumbricoides (35.9%),
T. trichiura (15.8%),
S. mansoni (11.7%), hookworm (9.8%),
T. saginata (3.9%),
H. nana (1.4%) and
Enterobius vermicularis (
E. vermicularis) (0.9%). Of the 378 intestinal helminth infected individuals, 35.8%, 13.3%, 4.3% and 0.6% had single, double, triple and quadruple infections, respectively. Intestinal helminth infection was most prevalent among individuals of age 5–15 years (63.2%).
A. lumbricoides and
T. trichiura infections were higher among individuals in 5–15 years age group than among individuals of age >15 years.
Table 2
Intestinal helminth infection among malaria suspected febrile patients Dore Bafeno Health Center, southern Ethiopia, December 2010
Age | | | | | | | |
<5 | 88 | 24 (27.3) | 2 (2.3) | 12 (13.6) | 3 (3.4) | 6 (6.8) | 35 (39.3) |
5–15 | 182 | 86 (47.3) | 10 (5.5) | 36 (19.8) | 24 (13.2) | 9 (5.0) | 115 (63.2) |
>15 | 432 | 142 (32.9) | 57 (13.2) | 63 (14.6) | 55 (12.7) | 15 (3.5) | 228 (52.8) |
χ2 (p) | | 14.76 (0.001) | 15.05 (0.001) | 2.96 (0.228) | 6.70 (0.035) | 5.96 (0.202) | 14.13 (0.001) |
Sex | | | | | | | |
Female | 341 | 135 (39.6) | 28 (8.2) | 65 (19.1) | 33 (9.7) | 19 (5.6) | 190 (55.72) |
Male | 361 | 117 (32.4) | 41(11.4) | 46 (12.7) | 49 (13.6) | 11 (3.0) | 188 (51.93) |
χ2 (p) | | 3.93 (0.047) | 1.96 (0.162) | 5.26 (0.022) | 2.58 (0.108) | 3.06 (0.217) | 1.02 (0.314) |
Mean intensity of infections were 2345 egg per gram {epg} (range; 24–16128) for A. lumbricoides, 372 epg (range; 24–12816) for S. mansoni, 107 epg (range; 24–1200) for hookworm and 101 epg (range; 24–1296) for T. trichiura. Intensity of A. lumbricoides infection showed age related pattern with the highest (F=3.36, p=0.036) mean intensity being observed among individuals of age group 5–15 years (mean epg=3113.7) followed by individuals of age group <5 years (mean epg=2410.6). Mean intensity of hookworm infection was higher (F=15.69, p<0.001) among individuals of age <5 years (mean epg=648) followed by those individuals whose age ranges from 5–15 years (mean epg=69.6).
Malaria and helminth co-infection
Out of 702 patients, 242 (34.5%) were infected with intestinal helminths alone, 86(12.3%) with
Plasmodium alone, and 136 (19.4%) with both
Plasmodium and intestinal helminths (Table
3). Intestinal helminthic infection was significantly associated with increased odds of malarial infection (i.e.
P. falciparum and/or
P. vivax infection) (unadjusted OR =1.56, 95% CI=1.13-2.16,
p=0.007). Prevalence of
P. falciparum infection was significantly higher in individuals infected with any intestinal helminth (s),
A. lumbricoides alone,
T. trichiura alone,
S. mansoni alone compared to those who were not infected with intestinal helminths (9.3%) (
p<0.001 for all) (Table
3).
Table 3
Prevalence of malaria and intestinal helminth co-infections among malaria suspected febrile patients who attended Dore Bafeno Health Center, southern Ethiopia, December 2010
Only A. lumbricoides (Al) | 141 | 30 (21.3) | 20 (14.2) | 2 (1.4) | 52 (36.9) |
Only hookworm (Hw) | 25 | 1(4.0) | 6 (24.0) | 0 | 7 (28.0) |
Only T. trichiura (Tt) | 39 | 9 (23.1) | 6 (15.4) | 0 | 15 (38.5) |
Only S. mansoni (Sm) | 39 | 9 (23.1) | 3 (7.7) | 0 | 15 (38.5) |
Al and Tt
| 42 | 9 (31.0) | 11 (35.5) | 2 (4.5) | 22 (52.4) |
Al and Sm
| 18 | 4 (22.2) | 1 (5.6) | 0 | 5 (27.8) |
Al, Tt and Sm
| 5 | 1 (20.0) | 1 (20.0) | 0 | 2 (40.0) |
Al, Tt, Sm and Hw
| 22 | 7 (31.8) | 1 (4.5) | 0 | 8 (36.4) |
Any intestinal helminth | 378 | 80 (21.2) | 51(13.5) | 5 (1.3) | 136 (36.0) |
Without intestinal helminths | 324 | 30 (9.3) | 50 (15.4) | 6 (1.9) | 86 (26.5) |
Out of 306 Plasmodium infected patients, 14 showed one or more sign and symptoms of severe malaria (i.e. prostration in 10 patients, breathing difficulty syndrome in 8 patients, cerebral malaria in 7 patients and severe anaemia in 3 patients). Nine severe malaria cases were volunteered to provide stool samples for the diagnosis of helminth infection and 7 of them were co-infected with intestinal helminths like A. lumbricoides, T. trichiura and hook worm.
Of the 292 non-severe malaria cases, 213 patients were examined for intestinal helminth infection and 61.0% were positive. The odds of non-severe malaria infection was higher in individuals infected with intestinal helminth compared to intestinal helminth-free individuals {adjusted Odds Ratio (AOR) =1.57, 95% CI= 1.12, 2.21}. Similarly, the odds of non-severe
P. falciparum mono-infection was higher among individuals infected with intestinal helminth than non-infected with intestinal helminth (AOR=2.89, 95% CI=1.77, 4.72). The ORs changed in parallel with the number of intestinal helminth species infection (p<0.001). Individuals infected with
A. lumbricoides alone (AOR=2.6),
T. trichiura alone (AOR=2.8),
S. mansoni alone (AOR=3.3), any intestinal helminth (AOR=2.9),
T. trichiura and
A. lumbricoides (AOR=3.1), and
T. trichiura,
A. lumbricoides,
S. mansoni and hookworm (AOR=4.0) had increased odds of non-severe
P. falciparum mono-infection compared to those who were not infected with any intestinal helminths (
p<0.05 for all) (Table
4). However, the proportions of
P. vivax mono-infected individuals were not significantly different when compared between those who had single or multiple infections with different intestinal helminths and intestinal helminth free individuals (data not shown). Similarly, infection with hookworm alone was not significantly associated with any of non-severe
P. falciparum and/or
P. vivax infection.
Table 4
Association of intestinal helminth infection and non-severe
P. falciparum
malaria among malaria suspected febrile patients who attended Dore Bafeno Health Center, southern Ethiopia, December 2010
P. falciparum
| Only A. lumbricoides (Al) | Crude | 2.58 | 1.44, 4.61 | 0.001 |
| | Adjusted* | 2.55 | 1.40, 4.63 | 0.002 |
| Only hookworm (Hw) | Crude | 0.47 | 0.06, 3.67 | 0.473 |
| | Adjusted* | 0.54 | 0.07, 4.35 | 0.565 |
| Only T. trichiura (Tt) | Crude | 2.48 | 0.98, 6.27 | 0.055 |
| | Adjusted* | 2.77 | 1.15, 6.65 | 0.023 |
| Only S. mansoni (Sm) | Crude | 2.83 | 1.21, 6.63 | 0.016 |
| | Adjusted* | 3.25 | 1.32, 7.97 | 0.010 |
|
Al and Tt
| Crude | 3.57 | 1.49, 8.55 | 0.004 |
| | Adjusted* | 3.12 | 1.27, 7.61 | 0.013 |
|
Al and Sm
| Crude | 2.44 | 0.75, 7.96 | 0.139 |
| | Adjusted* | 2.65 | 0.76, 9.22 | 0.125 |
|
Al, Tt and Sm
| Crude | 2.64 | 0.27, 26.23 | 0.406 |
| | Adjusted* | 2.34 | 0.23, 23.88 | 0.473 |
|
Al, Tt, Sm and Hw
| Crude | 3.96 | 1.48, 10.60 | 0.006 |
| | Adjusted* | 4.12 | 1.49, 11.31 | 0.006 |
| Any intestinal helminth | Crude | 2.74 | 1.71, 4.41 | 0.000 |
| | Adjusted* | 2.89 | 1.77, 4.72 | 0.000 |
Data regarding the effect of intestinal helminths co infection on malaria-related outcomes are summarized in Table
5. After adjusting for age, sex and nutritional status mean
Plasmodium density was significantly higher in individuals co-infected with four different intestinal helminth species (
T. trichiura,
A. lumbricoides,
S. mansoni and hookworm) compared to those who were free from intestinal helminth infection (β = 10829.56,
p<0.05). Similarly, there was an increasing trend in mean
Plasmodium parasitaemia among individuals who were infected with
T. trichiura alone,
S. mansoni alone,
A. lumbricoides alone and any two or three of these species compared to individuals who were not infected with any intestinal helminth species. The mean
Plasmodium density among intestinal helminth infected individuals increased significantly as the number of intestinal helminth species increased (F=2.82,
P=0.027). However, patients infected with hookworm alone showed slightly lower mean
Plasmodium parasitaemia compared to individuals who had no intestinal helminth infection.
Table 5
Effect of intestinal helminth infection on malaria related outcomes among microscopic confirmed malaria cases who attended Dore Bafeno Health Center, southern Ethiopia, December 2010 to February 2011
A. lumbricoides (Al) | 2.34 [−24.68, 20.00] | −0.52 [−1.37, 0.32] | 1.53 [0.72, 3.22] |
Hookworm (Hw) | −11.75 [−83.76, 60.26] | −0.65 [−2.64 , 1.34] | 1.69 [0.33, 8.81] |
S. mansoni (Sm) | 3.65 [−35.09, 42.41] | 0.12 [−1.45, 1.68] | 1.11 [0.30, 4.17] |
T. trichiura (Tt) | 19.11 [−13.31, 51.55] | −0.65 [−2.64 , 1.34] | 1.69 [0.33, 8.81] |
Al and Tt
| 15.16 [−21.34, 51.67] | -.63 [−1.77, 0.50] | 2.31 [0.80, 6.67] |
Al and Sm
| 22.19 [−55.82, 100.19] | -.08 [−2.68, 2.52] | 1.27 [0.17, 9.47] |
Al, Tt and Sm
| 64.65 [−10.53, 139.85] | −2.35 [−6.35, 1.63] | 2.83 [0.98, 15.24] |
Al, Tt, Sm and Hw
| 52.05 [5.08, 99.03] | −1.62 [−3.61, 0.37] | 8.64 [1.18, 63.47] |
Any intestinal helminth | 14.51 [−3.06, 32.07] | −0.34 [−0.99, 0.30] | 1.54 [0.81, 2.90] |
Individuals co-infected with A. lumbricoides, hookworm, S. mansoni, T. trichiura alone or in combination and Plasmodium showed lower mean haemoglobin levels compared to malaria cases without intestinal helminths infections. However, the mean differences were not significant in the multivariable model. Prevalence of anaemia was higher among individuals co-infected with both intestinal helminths and Plasmodium compared to those with Plasmodium infection alone. Individuals co-infected with Plasmodium and four different intestinal helminths were almost 9 times more likely to be anaemic compared to those with Plasmodium infection alone (AOR=8.64, 95% CI=1.18, 63.47).
There was not significant correlation between the mean Plasmodium density and intensity of intestinal helminth infections (spearman correlation coefficient= 0.12, -0.19, 0.04, -0.08 for A. lumbricoides, hookworm, T. trichiura, S. mansoni, respectively). In S. mansoni and T. trichiura infected patients, the mean parasitaemia increased as the class of intensity of the helminths increased; nonetheless the regression coefficients remain non-significant after adjusting for the effects of age, sex, nutrition, and concurrent infection by other species of helminth. Conversely, the mean parasitaemia of individuals with moderate intensity of A. lumbricoides infection was relatively low compared to individuals co infected with light intensity of A. lumbricoides and Plasmodium. For hookworm infection, all the infected cases were of light intensity class (data not shown).
The reduction in mean haemoglobin level among individuals co-infected with intestinal helminths and Plasmodium was negatively correlated with intensity of intestinal helminths. However, the coefficients for the association were low. Similarly, although the mean differences were not significant, haemoglobin levels decreased more in Plasmodium infected individuals co-infected with heavy intense S. mansoni or moderate intense T. trichiura infections compared to individuals with light intensity of infections with the respective intestinal helminths (data not shown).