Concomitant Plasmodium and helminth (S. haematobium and STHs) infections are common in parts of South-West Cameroon (8, 36, 37), due to geographic overlap of climatic and socio-economic conditions that support survival of the malaria parasite vectors, egg and larval development of STHs and Schistosoma sp. intermediate snail hosts. Monitoring the effectiveness of intervention programs in reducing disease prevalence and examining the roles behaviour, demography, and nutritional status play in the co-occurrence of parasitic infection as well as attributing morbidity-related outcomes is heartened. Following 8 years of MDA of praziquantel and albendazole to SAC, and the free distribution of LLIN to communities in the Mount Cameroon area [20 22, 23], we determined the prevalence and determinants of polyparasitism and evaluated the outcomes and clinical correlates of infections in SAC living in the schistosomiasis endemic foci of Bafia, Ikata and Likoko.
Polyparasitism occurred in 19.9% of the children although the prevalence of single infection was more common with similar occurrence of S. haematobium and P. falciparum infection. This polyparasitism prevalence in SAC is higher than the 7.6% observed in Mbam and Inoubou Division, within the Centre Region of Cameroon [38], 11.2% in Ghana [39] and lower than the 30% and 28% observed in Kenya [40, 41]. When compared with previous studies in the same locality [25, 42], a decline in infections with S. haematobium and P. falciparum following MDA was observed in SAC. However, the prevalence of polyparasitism is likely to remain a significant public health problem in the Ikata-Likoko area where environmental (streams near homes, high rainfall) and socio-economic (farming and fishing activities, inadequate health care services, low level of education) characteristics are likely to favour the transmission of these infections. Again, while the national control strategy for helminth infection in SAC may curb transmission, infected individuals not included in the programme are likely to serve as a source of re-infection due to their common exposure to snail infested streams serving the communities.
The predominance of S. haematobium and P. falciparum (7.8%) co-infection when compared with S. haematobium and STH (0.8%), MP and STH (0.8%) and S. haematobium, P. falciparum and STH (0.9%) is not unusual. This may be attributed to the significant decline in STH infections in the Mount Cameroon area following the school-based deworming (SBDW) strategy with mebendazole adapted by Cameroon in 2004 and has been implemented annually since 2007 in both enrolled and unenrolled children [43; 44]. This S. haematobium and P. falciparum co-infection is of public health importance as the prevalence is higher than the 0.9% observed in Accra Ghana [45], comparable to the 9.0% in Gabon [46], lower than the 10.9% and 13.6% reported in Mvomero-Tanzania and West Region of Cameroon respectively [47, 48] and within the 2.84 to 57.1% range reported in Africa [16, 49, 50].
Findings from the univariate analysis revealed being female, site (Likoko), children who did not use potable water, usually bathed in streams and carried out open defecation were more likely to have S. haematobium and Plasmodium co-infection with interchangeable factors affecting the prevalence of P. falciparum and STH. Similar factors have been reported elsewhere [9, 46, 51]. However, the multivariate analysis demonstrated being female was the only significant risk factor with 2.38 times likelihood of having the S. haematobium and Plasmodium co-infection. This is not surprising as females spend more contact time in infested streams washing clothes, playing, swimming, and when bathing hence, the likelihood to be re-infected after treatment is higher [52, 53]. Albeit S. haematobium and P. falciparum have distinct transmission patterns, findings from the study (Additional file 2) demonstrated similar drivers of the infections. This probably asserts the influence of environmental and host factors on the epidemiological and geographical patterns of infections and diseases [54]. Hence, sustainable multidisciplinary intervention that integrates preventive chemotherapy with education on water, sanitation and hygiene (WASH), provision of potable water supply to communities, appropriate faecal disposal methods and improvement in health facilities and care is desired to reduce the burden of parasitic infections.
Worthy of note is the abundance of light infections with S. haematobium and low-density malaria parasite infections observed. In addition, all infections with STHs (Ascaris lumbricoides and Trichuris trichuria) were light and occurred mostly in SAC of Likoko area. The consequences of the absence of potable water supply and an integrated health centre in the Likoko community is undoubtedly demonstrated here by the presence and high occurrence of all the identified parasites, suggestive of contaminated environment than the other localities. The high prevalence of light infection is consistent with similar studies in Nigeria, Malawi and Ghana [45, 52, 55]. Light infections can occur in populations previously targeted for schistosomiasis control [56] on the other hand, high prevalence of heavy intensity infection suggestive of long-term transmission and attributable to poor sanitation and water supply facilities have also been reported [57]. Most likely, the MDA with an anti-helminthic each year and the ineffective use of the LLIN were not successful in preventing reinfections but probably aided in maintaining lower grade parasite intensities in the population.
Low levels of parasite loads represent chronic parasite infections which may play a major role in clinical morbidity [58]. The effects of polyparasitism which are often clinically inapparent may lead to multiple morbidities. Nevertheless, in some situations, co-infections may exacerbate disease symptoms due to one of the pathogens. Observations from the study revealed anaemia as the most common (74.3%) clinical morbidity measured and its occurrence was exacerbated in co and triple infections with Plasmodium and helminths in line with Nyarko et al [45]. Furthermore, a slight agreement in sensitivity and specificity of anaemia with microscopy in predicting the presence of both S. haematobium and P. falciparum infections was proven. While the spectrum of anaemia is broad and complex in resource-limited settings, these findings assert the significant contributions of urogenital schistosomiasis and malaria to the burden of anaemia in endemic areas accentuated by several studies [50, 59, 60] and could be a valuable presumptive diagnostic marker of both infections even if the specificity is low.
Morbidity associated with urogenital schistosomiasis is caused by granulomatous reactions formed in response to egg deposition in the walls of the urinary tract, triggering inflammatory reaction, haematuria, proteinuria, fibrosis with ensuing obstruction and bladder carcinogenesis
(61, 62). Haematuria or bloody urine is a classic sign of urogenital schistosomiasis and findings from the study revealed an overall prevalence of 13.0%. This is lower than the 16.6% observed in SAC in Northern Angola [63]. Haematuria was the second most common morbidity associated with urogenital schistosomiasis with 100% specificity, sensitivity of 46.5% and a moderate kappa agreement with microscopy in predicting the presence of the infection. The high specificity and low sensitivity observed is not atypical even though the sensitivity is lower than the 65% reported in populations with lower intensity infections [64]. Nonetheless, this is congruent with synthesis of previous findings that highlight dipstick sensitivity to decrease while specificity increases when compared to dipstick performance in high prevalence areas. This lends support for the need of a combination of diagnostic tools including clinical criteria as light and old infections may be missed by microscopy [65].
Other morbidities of significance observed in the study were microcytosis (45.3%) and malnutrition (26.5%). The prevalence of malnutrition (24.4%), with the most common being stunting, is comparable to those of SAC in localities close by [66] and lower than the 29.7% in SAC in Rural Senegal [67]. Observation from the study showed a general inclination of SAC with P. falciparum to have predominance of microcytosis while those with S. haematobium had a higher occurrence of malnutrition. Unlike the increase in prevalence of microcytosis observed in P. falciparum and S. haematobium co-infection, increase in malnutrition prevalence was observed in triple infections of S. haematobium, P. falciparum and STH only. Although the directionality of causality of these morbidities are not very specific, microcytosis have been previously associated with protection against erythrocytic stage Plasmodium infection and severe malarial anaemia [68, 69]. On the other hand, the growth faltering and malnutrition attributed to urogenital schistosomiasis has been linked to chronic anti parasite inflammation which persists during childhood [67, 70, 71, 72].
A history of fever in the past 3 days was the most common unmeasurable clinical outcome reported while fever pervasiveness was lower. In addition, co-infection with S. haematobium and malaria parasite was significantly associated with 3-fold odds of history of fever in the last three days. Fever is a non-specific marker of infection that is often considered as a symptom of malaria in endemic areas. It results from endogenous pyrogen molecules activities, notably pro-inflammatory cytokine tumour necrosis factor (TNF)-α. However, S. haematobium infection could further augment anti-inflammatory responses induced by asymptomatic P. falciparum infection reducing the risk of fever probably accounting for the low occurrence of fever in the population [46, 73]. Other common morbidities of significance reported associated with co-infections include lower abdominal pain, diarrhoea and vomiting.
The study is not without limitations. The use of a single stool and urine sample for the detection of helminth infection may have led to underestimation of the prevalence of polyparasitism as well as the intensities of the infections considering the variation in day to day excretion of eggs of some of these parasites. Other intestinal parasites may have gone undetected due to the insensitivity of the Kato-Katz technique used. Despite this underestimation, we consider the data meaningful to reveal implications on disease-related outcome and clinical correlates.