Abstract
Background
Rapid and accurate diagnosis is necessary for the management of schistosomiasis in endemic areas.
Objective
To assess the burden of urogenital schistosomiasis and the diagnostic efficiency of morbidity indicators of the disease in an endemic rural community of Nigeria.
Methods
A cross-sectional school-based study was conducted. Urine samples of 487 pupils were screened microscopically for S. haematobium and tested for haematuria and proteinuria using chemical reagent strips.
Results
The prevalence and intensity of infection were 57.1% and 45.0 eggs/10 mL urine respectively. Prevalence of infection in male (54.1%) and female (60.3%) individuals showed no significant variation (P>0.05). However, prevalence of infection was age dependent with those in age groups 3–5 and 12–14 years having the least and highest prevalence of infection respectively (P<0.05). Microhaematuria and proteinuria varied significantly with ages of the pupils with least (14.0, 40.0%) and highest (60.0, 80.0%) prevalence recorded in age groups 3–5 and 15–19 years respectively (P<0.05). Proteinuria showed higher sensitivity (80.3%) compared to microhaematuria (73.3%).
Conclusion
Schistosomiasis is highly endemic in the study area and the use of microhaematuria and proteinuria for mapping the infected population prior treatment could be adopted.
Keywords: Schistosomaisis, haematuria, proteinuria, Nigeria
Introduction
Schistosomiasis is a chronic disease with high public health importance as 207 million people have been estimated to be infected worldwide1. Most recent estimate reported 50.8 million infected individuals in aged ≤ 20 years in West Africa2 (Schur et al., 2011). Schistosomiasis has been widely reported in Nigeria3–6.
The implementation of programmes to controlschistosomiasis requires up-to-date information regarding the prevalence and distribution of the diseases7. Rapid and indirect diagnostic methods have been suggested to aid quick mapping surveys in endemic regions8.
This becomes important as rapid detection of diseased individuals is necessary for efficient intervention through mass drug administration in the areas. Some of the notable indicators of infection especially due to S. haematobium for rapid assessment are haematuria, proteinuria and leukocyturia.
Operational research studies in Nigeria and other African countries have shown these indicators as good morbidity indicators of S. haematobium infection and have been successfully used to identify school children requiring treatment and subsequently monitor control9,10. However, the low sensitivities of these indicators to detect the diseased population especially in low endemic areas have raised some questions on the reliance of results obtained from such studies. An approach of combining two or more indicators has been developed to improve the diagnostic accuracy or efficiency10.
The present school-based study reports the prevalence of urogenital schistosomiasis and reliability of haematuria and proteinuria as diagnostic indicators of the disease in a rural endemic area of Nigeria.
Materials and methods
Study setting
A cross-sectional school based study was conducted in Yewa North Central Primary School, Ijoun, Ogun State in the south-western part of Nigeria. Ijoun is a rural community with a heterogeneous population comprising the Yorubas, Fulanis, Igbos and few individuals from the Republic of Benin. The inhabitants depend on streams and rivers for their sources of water for domestic purposes. The snail intermediate hosts of S. haematobium have been discovered in the river bodies in the area11.
Sample size and sampling procedures
Sample size was calculated using the method described by Naing et al.12 A prevalence of 55% was used to compute the minimum sample size based on previous report on schistosomiasis in some other communities in the LGA13. The sample size arrived at was 380 with precision 0.05(5%) being the most suitable. The statistical power used was 80%. A total of 541 school pupils were recruited but 487 and 432 pupils provided urine samples for microscopic examination and reagent strips screening respectively. Class to class recruitment procedure was adopted during which the pupils through the help of the class teacher were given urine sample bottles and were monitored for urine collection. Samples were collected between March and April, 2010.
Data collection
Clean and sterile universal urine containers were given to each of the pupils to collect samples of urine. Urine, 10–20 mL, was collected at midday (10.00–14.00 hours) under the proper guide of the teachers and the research team. The urine containers were clearly labelled with the sample number assigned to each participant.
The freshly passed urine samples were inspected macroscopically for gross haematuria and then screened for microhaematuria and proteinuria using commercially available urine reagent strips (Medi-Test Combi 10, Standard Diagnostics Inc., Korea). The strip testing was performed in accordance with the manufacturer's instructions. The urinary protein content was recorded as negative (< 0.1g/L of urine), trace (<0.3g/L), 1+, 2+, 3+ or 4+. The symbols are intended to correlate as follows: +1 with 0.3 g/L, +2 with 1.0 g/L, +3 with 3.0 g/L and +4 with ≥5.0 g/L. The samples were transported in a dark container to the laboratory and processed within 24 hours after collection. Each sample was well-mixed and 10 mL was withdrawn using clean, sterile plastic syringes. This was then centrifuged at 5000 rpm for 5 minutes. The supernatant was decanted and the sediments were transferred to a clean slide and examined under a light microscope for eggs of S. haematobium using the x10 objective lens.
Intensity of infection was classified using Briand et al.'s modification of WHO recommendations14. Intensity of infection was thus categorized as no infection, light infection (1–9 egg/10mL of urine), moderate infection (10–49 eggs/10 mL of urine) and heavy infections (≥50 eggs/10 mL of urine). All the infected individuals were treated with single dose of 40 mg/kg of praziquantel.
The older pupils were asked their ages while in case of uncertainty and in younger pupils, the class teachers were engaged who confirmed their ages by consulting the class register containing each pupil bio-data. The age of each pupil was recorded against their names in the register created for the study.
Quality control
Urine samples collected were prevented from direct light penetration in order to avoid hatching of parasite eggs before microscopy examination. Parasite morphology and intensity was confirmed by another scientist during examination.
Ethical considerations
Ethical approval was obtained from the joint University of Ibadan/University College Hospital Ethical Review Board. Approval was also obtained from Ogun State Ministry of Health and the Ministry of Education. The community's leaders and the school's administrators were duly informed of the objectives and benefits of the study. The children parents were also invited to Parent Teacher Association (PTA) meeting during which they were briefed on the significance of the study. Written informed consent was obtained from them after a detailed explanation of the objectives of the study. Participant's personal information was treated private and was not divulged to third party. For example, sample bottles were identified only by a unique code allotted to them while every other information was recorded in the study's register.
Inclusion and exclusion criteria
All pupils with the exception of the very few ones who declined were recruited for the study.
Statistical analysis
Data were entered into an Excel spreadsheet, checked for entry errors and transferred into SPSS for Windows (version 15.0, SPSS Inc, Chicago, USA) for analysis. The sensitivity (number of individuals with a positive rapid test/individuals with a positive reference test) and specificity (number of individuals with a negative rapid test/individuals with a negative reference test) were calculated for rapid tests (chemical reagent strips) compared to the gold standard (microsscopy was used as the reference test). Chi-square tests were applied to compare relative proportions of infections between genders and ages of the pupils. When analyzing for the effect of age, pupils were divided into 5 groups: aged 3–5, 6–8, 9–11, 12–14, and ≥ 15 years. The intensity of infection measured by the parasite egg counts was logarithmically transformed into geometric mean. Student's t-test and ANOVA were used to determine significant differences in intensity of infection. P values < 0.05 were considered significant.
Results
The overall prevalence and intensity of infection due to S. haematobium were 57.1% and 45.0 eggs/10 mL urine (OR=1.8, CI=1.1–3.8) respectively. Prevalence of urogenital schistosomiasis varied significantly across age groups (P<0.05) with the least (27.5%) (OR=0.5, CI=0.3–1.0) and highest prevalence (68.4%) (OR=2.9, CI=2.0–4.2) recorded in age groups 3–5 and 12–14 years respectively (Table 1).
Table 1.
Age and sex related infection pattern
| Age group (years) |
Sex | No. examined | No. infected (%) |
Light infection (%) |
Moderate infection (%) |
Heavy infection (%) |
OR(95%CI) |
| 3–5 | M | 32 | 7(21.9) | 3(42.9) | 1(14.3) | 3(42.9) | 0.5(0.1–1.7) |
| F | 19 | 7(36.8) | 2(28.6) | 0(0) | 5(71.4) | 2.1(0.6–7.3) | |
| T | 51 | 14(27.5) | 5(35.7) | 1(7.1) | 8(57.1) | 0.5(0.3–1.0) | |
| 6–8 | M | 65 | 33(50.8) | 7(21.2) | 14(42.2) | 12(36.4) | 1.4(0.7–2.8) |
| F | 58 | 25(43.1) | 7(28.0) | 10(40.0) | 8(32.0) | 0.7(0.4–1.5) | |
| T | 123 | 58(47.2) | 14(24.1) | 24(41.4) | 20(34.5) | 1.2(0.8–1.8) | |
| 9–11 | M | 64 | 36(56.3) | 7(19.4) | 12(33.3) | 17(47.2) | 0.6(0.3–1.1) |
| F | 72 | 50(69.4) | 8(16.0) | 13(26.0) | 29(58.0) | 1.8(0.9–3.6) | |
| T | 136 | 86(63.2) | 15(17.4) | 25(29.1) | 46(53.5) | 2.3(1.5–3.4) | |
| 12–14 | M | 81 | 52(64.2) | 3(5.8) | 20(38.5) | 29(55.8) | 0.7(0.3–1.3) |
| F | 71 | 52(73.2) | 14(26.9) | 11(21.1) | 27(51.9) | 1.5(0.8–3.0) | |
| T | 152 | 104(68.4) | 17(16.4) | 31(29.8) | 56(53.9) | 2.9(2.0–4.2) | |
| ≥15 | M | 13 | 10(76.9) | 1(10.0) | 5(50.0) | 4(40.0) | 3.3(0.6–18.5) |
| F | 12 | 6(50.0) | 1(16.7) | 1(16.7) | 4(66.7) | 0.3(0.1–1.7) | |
| T | 25 | 16(64.0) | 2(12.5) | 6(37.5) | 8(50.0) | 2.3(1.0–5.5) | |
| Total | M | 255 | 138(54.1) | 21(15.2) | 52(37.7) | 65(47.1) | 0.8(0.5–1.1) |
| F | 232 | 140(60.3) | 32(22.9) | 35(25.0) | 73(52.1) | 1.3(0.9–1.8) | |
| T | 487 | 278(57.1) | 53(19.1) | 87(31.3) | 138(49.6) | 1.8(1.1–3.8) |
Note: OR- odd ratio, CI- confidence interval
There was no gender difference in infection pattern (P>0.05), however, more female participants (60.3%) (OR=0.8, 0.5–1.1) were infected than the male participants (54.1%) (OR=1.3, CI=0.9–1.8). The overall prevalence of microhaematuria was 50.0% and age related prevalence of microhaematuria was similar to what was observed in infection due to S. haematobium with the least (14.0%) and highest (60.0%) prevalence recorded in age groups 3–5 and 12–14 years respectively (Table 2).
Table 2.
Age and sex prevalence profiles of urogenital schistosomiasis morbidity indicators
| Age group (years) |
Sex | Macrohaematuria | Microhaematuria | Proteinuria | ||
| No. | Prevalence | No. | Prevalence | Prevalence | ||
| examined | (%) | examined | (%) | (%) | ||
| 3–5 | M | 32 | 1(3.1) | 31 | 4(12.9) | 14(45.2) |
| F | 19 | 0(0.0) | 19 | 3(15.8) | 6(31.6) | |
| T | 51 | 1(2.0) | 50 | 7(14.0) | 20(40.0) | |
| 6–8 | M | 65 | 11(16.9) | 55 | 20(36.4) | 33(60.0) |
| F | 58 | 12(20.7) | 51 | 25(49.0) | 21(41.2) | |
| T | 123 | 23(18.7) | 106 | 45(42.5) | 54(50.9) | |
| 9–11 | M | 64 | 16(25.0) | 51 | 28(54.9) | 37(72.5) |
| F | 72 | 11(15.3) | 55 | 34(61.8) | 36(65.5) | |
| T | 136 | 27(19.9) | 106 | 62(58.5) | 73(68.9) | |
| 12–14 | M | 81 | 16(19.8) | 78 | 45(57.7) | 65(83.3) |
| F | 71 | 8(11.3) | 67 | 42(62.7) | 49(73.1) | |
| T | 152 | 24(15.8) | 145 | 87(60.0) | 114(78.6) | |
| ≥15 | M | 13 | 3(23.1) | 13 | 7(53.9) | 12(92.3) |
| F | 12 | 2(16.7) | 12 | 8(66.7) | 10(83.3) | |
| T | 25 | 5(20.0) | 25 | 15(60.0) | 22(88.0) | |
| Total | M | 255 | 47(18.4) | 228 | 104(45.6) | 161(70.6) |
| F | 232 | 33(14.2) | 204 | 112(54.9) | 122(59.8) | |
| T | 487 | 80(16.4) | 432 | 216(50.0) | 283(65.5) | |
Microhaematuria varied significantly across age groups (P<0.05) but showed no significant variation with gender (P>0.05). The overall prevalence of proteinuria is 65.5% with the least (40.0%) and highest (88.0%) prevalence recorded in age groups 3–5 and 15–19 years respectively. The difference in prevalence of proteinuria between age groups was statistically significant (P<0.05). Prevalence of proteinuria was significantly higher in male subjects (70.6%) than in the female subjects (59.8%) (P<0.05). The overall proportion of the population with proteinuria ranging from none (<0.1 g/L) to trace urinary quantity (<0.3 g/L) was 48.5% while 51.5% of the population had proteinuria ≥0.3 g/L. Most of the male subjects showed higher proportion of pathologic urinary proteinuria (56.3, 65.7, 100%) than their female counterparts (43.8, 34.3, 0.0%) in the 0.3, 3.0, 5.0 g/L categories respectively (Table 3).
Table 3.
Severity of proteinuria in the study population (n=210)
| Proteinuria Gradients (g/L) |
Male Number (%) |
Female Number (%) |
Total (overall %) |
| <0.1(-ve) | 10(31.3) | 22(68.8) | 32(15.2) |
| <0.3(Trace) | 46(65.7) | 24(34.3) | 70(33.3) |
| 0.3(1+) | 36(56.3) | 28(43.8) | 64(30.5) |
| 1.0(2+) | 23(65.7) | 12(34.3) | 35(16.7) |
| 3.0(3+) | 1(100) | 0(0.0) | 1(0.5) |
| 5.0(4+) | 4(50.0) | 4(50.0) | 8(3.8) |
| Total (n) | 120 | 90 | 210 |
The most sensitive (80.3%) Schistosoma morbidity indicator was proteinuria while macrohaematuria was the least sensitive (24.8%) indicator of infection due to S. haematobium. However, microhaematuria which recorded higher values in other diagnostic parameters compared to proteinuria showed overall highest diagnostic accuracy of 76.2% (Table 4).
Table 4.
Diagnostic performance of indirect screening methods used for urogenital schistosomiasis
| Diagnostic Parameters | ||||||
| Diagnostic Predictors | Sensitivity | Specificity | PPVa | NPVb | Accuracy | Reliability |
| Macrohaematuria | 24.8 | 94.7 | 86.3 | 48.7 | 54.8 | 0.144 |
| Microhaematuria | 73.3 | 80.0 | 82.4 | 69.9 | 76.2 | 0.531 |
| Proteinuria | 80.3 | 53.4 | 68.9 | 67.8 | 68.5 | 0.337 |
| Microscopy | 100 | 100 | 100 | 100 | 100 | 1.000 |
Note
positive predictive value,
negative predictive value
Discussion
The results of this study confirm the active transmission of S. haematobium in the study area. The public health implication of the disease is high enough to attract appropriate interventions like mass drug administration and provision of safe water. The overall prevalence of urogenital schistosomiasis (57.1%) reported in this study is higher than Nigerian estimated mean prevalence 39.1%2 and records from other African countries15,16. In moderate-to-high Schistosoma endemic regions, infection usually varies with age and gender. The heterogeneity in exposure influenced by behaviour, culture and social factors, the development of acquired immunity, as well as, physiological changes during puberty are factors that influence susceptibility to the parasite17. It is therefore of particular note that in the study area, this typical age-related profile of egg-positive cases appeared, being concordant with a typical endemic area. The age-related infection pattern is similar to other studies conducted in Nigeria18,19 but clearly deviated from other studies that reported significant differences in sex-related prevalence3. The lack of association between infection and ages of the subjects could be due to equal dependent on natural water bodies in such low resource community with poor water development.
The high prevalence of microhaematuria and proteinuria is similar to a study conducted in Minna, Niger State, Nigeria20. These two morbidity indicators are recognized clinical features of S. haematobium infection21. Both symptoms are indicators of damage in the urinary tract and kidney20. Inconclusive evidence has suggested S. haematobium associated glomeruli pathology. When the glomeruli are damaged, protein and often red blood cells leak into the urine. Although, at the present, the precise origin and clinical significance of the proteinuria observed in S. haematobium infection remains unknown22. High prevalence of glomerulonephritis had been reported in areas of the tropic where urogenital schistosomiasis is also common, however its relationship to S. haematobium remain unclear23. The occurrence of high proportion of pathologic urinary proteinuria (≥0.3 g/L) in the current study may suggest urogenital schistosomiasis involvement in inducing glomeruli pathology resulting in abnormal urinary protein excretion. This effect being more pronounced in the male subjects could be due to higher intensity of infection due to S. haematobium in the group compared to their female counterparts.
The degree of microhaematuria and proteinuria detectable by chemical reagent strip observed to correlate significantly with microscopy is also similar to the findings18. The association of these symptoms with urogenital schistosomiasis had been widely documented24–26. The high sensitivity for haematuria and proteinuria reported in this study conforms favourably with earlier reports27–29. Macrohaematuria was the most specific but least sensitive, although it has the benefit of not requiring reagent strips. Its gender disparity, however, needs to be considered if using this test, with females requiring additional test30.
The inability to generalize result in other population groups since the participants constituted only school pupils and use of single urine sample for both microscopy and morbidity screening are the potential limitations of the study.
The present study shows that microhaematuria is the most accurate and reliable indirect diagnostic method. This is as a result of its high specificity for negative results and high positive predictive value for positive results. The high sensitivity values reflect the usefulness of these diagnostic indices as morbidity indicators of S. haematobium in an endemic area. It is also worth mentioning that a combination of proteinuria and microhaematuria may be more efficient in infection diagnosis than a single variable.
Acknowledgements
This study is financed by MacArthur Multidisciplinary Grant of University of Ibadan, Ibadan, Nigeria. Many thanks to the Education Authorities of Yewa North Local Government Area of Ogun State, Southwestern Nigeria, Head Teachers, parents and pupils of the participating schools for permission to carry out this study.
References
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