JSM Tropical Medicine and Research

Is it Time to Reconsider Serological Approaches for the Diagnoses and Surveillance of Schistosomiasis in Endemic Areas under Control? Contributions of a Field Research in a Brazilian Low Endemic Area

Short Communication | Open Access

  • 1. Department of Tropical Medicine, Federal University of the Triângulo Mineiro, Brazil
  • 2. Department of Collective Health, University of Brasília, Brazil
  • 3. Biohelmintiasis Section, Central University of Venezuela, Venezuela
  • 4. Department of Tropical Medicinre, Triângulo Mineiro, Brazil
  • 0. In memoriam
+ Show More - Show Less
Corresponding Authors
Raiza Ruiz-Guevara, Department of Tropical Medicine, Federal University of the Triângulo Mineiro, Brazil, Tel: 58-212-6053587

We conducted this study for assessing the field diagnostic accuracy and usefulness of Kato-Katz coprological test, the enzyme-linked immunosorbent assay with soluble egg antigen of Schistosoma mansoni modified by sodium metaperiodate (SMP-ELISA) and the circumoval precipitin test (COPT), for the detection of schistosomiasis infection in a low endemic area of Brazil.

Methods: Survey was conducted in northwest Brazil and was done using as reference standard a single Kato-Katz slide, similar to the used routinely in endemic areas in previous studies. The accuracy of SMP-ELISA and the COPT, used simultaneously or in a sequential (two-stage) form was evaluated.

Results: With a single Kato-Katz smear the schistosomiasis prevalence was 1.8%, by SMP-ELISA prevalence was31% and COPT 27.4%. SMP-ELISA showed high sensitivity (95.2%) and COPT best specificity (75.2%). When we use simultaneous SMP-ELISA and COPT, there was a net gain in sensitivity but a net loss in specificity. When SMP-ELISA was used as initial screening test and positives were re-tested with COPT there was a net loss in sensitivity but a net gain in specificity.

Conclusion: For epidemiological surveys we suggest the use of an easy, fast and cost-effective test as SMP-ELISA as initial screening method; the positives should be tested again with a specific confirmatory technique such as the COPT to identify real positives. Maybe, in those COPT positive persons, it might be useful to emphasize the search of S. mansoni eggs.


Ruiz-Guevara R, Prata A, Urdaneta M, Merchán-Hamann E, Losada S, et al. (2016) Is it Time to Reconsider Serological Approaches for the Diagnoses and Surveillance of Schistosomiasis in Endemic Areas under Control? Contributions of a Field Research in a Brazilian Low Endemic Area. JSM Trop Med Res 1(2): 1012.


•    Schistosomiasis mansoni
•    Low endemicity
•    Serology
•    Kato-Katz
•    Brazil
•    Diagnostic accuracy


When specific schistosomiasis control measures are applied in endemic areas, the true prevalence of remaining cases is difficult to assess through coprological studies [1,2] because the intensity of Schistosoma mansoni infection decreases; however these infected people with very low parasitic loads, are able to keep the transmission [3,4]. The method recommended by the World Health Organization (WHO) for the diagnosis of S. mansoni infection [5] is the Kato-Katz coprological test, which is reasonably sensitive in high endemic areas, relatively simple and inexpensive, even under field conditions [6]. However, it loses sensitivity when used in low endemic areas where patients have few numbers of eggs in stools [7-11]; especially when only one sample stoolis done. In consequence, the results and impact of intervention measures are difficult to assess and interpret [3].

Priorities of control measures vary according to endemicity and program development [12]. In highly endemic areas the priority is the reduction of morbidity and mortality [13,14]. In low endemic areas, where infected individuals with low egg loads predominate, the interruption of the transmission is the most important goal. Therefore, sensitivity of the diagnostic method is crucial [9,15] and precise diagnosis of schistosome infections will play a pivotal role in achieving these goals [16]. Moreover, Brazilian researches emphasize the need of the study of new or combined methodology to evaluate if there is successful disease elimination and its surveillance in endemic countries [17].

An alternative way to diagnose schistosomiasis is through the detection of antigens or antibodies against S. mansoni. However, the study of antigenemy has not proven to be sensitive enough in low transmission areas [18].

Under these circumstances of low endemicity and limited sensitivity of both parasitologic and antigen determination, immunological techniques for detection of antibodies may be the best available methods for diagnosis. Several studies suggest that in areas of low intensity of infection, the sensitivity and specificity of methods such as the enzyme-linked immunosorbent assay with soluble egg antigen of S. mansoni modified by sodium metaperiodate (SMP-ELISA) and the circumoval precipitin test (COPT), appear to be satisfactory [19-24]. Moreover, researchers from Brazil and China use COPT as a gold standard in the diagnosis of S. mansoni-infection in low endemicity areas due to its high sensitivity and specificity[25,26].

When patients eliminate large quantities of S. mansoni eggs and they are easily found by performing one fecal examination, it was not necessary to assess the serologic tool. Such is the case of Brejo do Espírito Santo in the interior of Bahia (Brazil) where initial studies in 1976 found a prevalence of infection of 75.4% with an arithmetic mean of 802.5 (24-21360) eggs per gram of feces [27]. After the introduction of control measures of schistosomiasis, between 1980-1997, preliminary observations made between 2002-2003 suggest that there has been a significant reduction in both the prevalence (1.8%) and intensity of infection (a mean of 45.6 eggs per gram of stool) [27]. It is possible that the true prevalence of schistosomiasis in Brejo do Espírito Santo would be greater if serology was used. It is the case of Venezuela and China, where control programs have been successfully implemented and its assessment is based on coprologic and serologic tests [22,28,29].

We conducted this study with the goal of assessing the field diagnostic accuracy and usefulness of Kato-Katz coprological test, and SMP-ELISA and COPT serological tests, for the detection of schistosomiasis infection in a low endemic area of Brazil.


Study area. The study setting was Brejo do Espírito Santo, a rural area in the municipality of Santa Maria da Vitória, located at the southwest of the State of Bahia (Brazil), approximately 580 km away from Brasília.

Field work and laboratory procedures

a. In this work all of the 3,164 residents of Brejo do Espírito Santo were interview. Forty five percent of the interviewees (1,428) provided a single stool sample, from which one smear was prepared and evaluated at site by the Kato-Katz method [30]. The arithmetic mean of egg output was calculated and expressed as eggs per gram of feces. Parasitological tests were performed by the staff of the Regional Direction of Health of Santa Maria da Vitória within 24-48 hours after collection.

b. We collected also an additional 5 ml blood sample for serologic assays from 1,325 people. Serum samples were kept in ice and then frozen to -80o C until processing at the Sección de Biohelmintiasis of the Institute of Tropical Medicine (Venezuela) where the immunological diagnosis of schistosomiasis was blindly made by means of enzyme-linked immunosorbent assays with soluble egg antigen of S. mansoni, modified by sodium metaperiodate (SMP-ELISA), as described by Alarcón de Noya et al., [31]. In those positive samples and in a subset of negative for SMP-ELISA, the circumoval precipitin test (COPT) was carried out [32]. Paired examinations of feces and blood samples were available in 521 participants and were classified in four patterns of combined serological results (Groups A, B, C and D) (Figure 1).

c. The parasitological history of this population obtained in earlier surveys conducted between 1976-1989 was available and reviewed in order to identify previous infection.

Data analysis

For the statistical analysis, SPSS 19 for Windows (Version 19.0; Copyright SPSS Inc., 2010) was used. All variables under study (except the parasitic load) were expressed as categorical variables and grouped in contingency tables:

a. Prevalence measurement. We calculated the prevalence of S. mansoni infection for: one stool examination and immunological serological tests.

b. Measures of diagnostic accuracy. The following measures of diagnostic accuracy were estimated: sensitivity, defined as the proportion of S. mansoni egg carriers who were correctly identified by the serological tests; specificity, defined as the proportion of negative participants to S. mansoni eggs correctly identified by the tests; positive and negative predictive values (PPV, NPV), defined as proportion of participants who tested positive and were true carriers and proportion of participants who tested negative and were true non carriers, respectively. Positive and negative likelihood ratios (PLR, NLR) for dichotomous variables were also estimated as: PLR = sensitivity/ (1–specificity) and NLR = (1–sensitivity)/specificity for each test [33]. For each measure the 95% Confidence Interval (95%CI) was calculated.

c. Reference standards. In this study, we evaluated the immunodiagnostic accuracy using as reference one stool sample (as routinely done in the field) and similar to Prata et al., in the past 29 years [27].

d. Multiple testing. Based on results of sensitivity and specificity of serological proves for the reference standard, we calculated the diagnostic accuracy parameters for the multiple uses of the immunodiagnostic tests, as follows:

i. For the simultaneous use of ELISA and COPT, net sensitivity was calculated as, Sensitivity test 1 + Sensitivity test 2 - (Sensitivity test 1 x Sensitivity test 2), and, the net specificity as, Specificity test 1 x Specificity test 2. PLR and NLR were calculated using net sensitivity and net specificity results.

ii. For the sequential (two-stage) use of ELISA and COPT, the test with best sensitivity was chosen as initial screening test followed by the test with best specificity. Net sensitivity was calculated as, Sensitivity test 1 x Sensitivity test 2, and, net specificity as, Specificity test 1 + Specificity test 2 – (Specificity test 1 x Specificity test 2). PLR and NLR were calculated using net sensitivity and net specificity results.

Ethical considerations

This study protocol was approved by the Ethics Committee in Research in the Faculty of Medicine of TriânguloMineiro (FMTM), Scientific Ethics Committee of the Institute of Tropical Medicine of the UCV, and the National Council of Ethics in Research (CONEP) in Brasilia. Each patient or legal representative signed, after reading the term of free and informed consent, as for to collect the coprological and the serological samples. All results were delivered house by house.


Study population and results of laboratory procedures

The demographic characteristics of population are described in Table (1), as well as their previous status of schistosomiasis infection and sickness. Among the 3,164 initially interviewed, 1,428 made the coprological study which showed S. mansoni eggs in 26 (1.8%) of them (arithmetic mean 45.6 ± 54.9 eggs per gram of feces). SMP-ELISA was positive in 412 out of 1,328 (31%) collected samples; the COPT performed in 558 individuals resulted positive in 153 (27.4%) (Figure 1).

Outcomes of paired samples (n = 521) were classified according to their results in four groups: 142 (27.3%) had positive SMP-ELISA and positive COPT (Group A); other 222 (42.3%) had positive SMP-ELISA and negative COPT (Group B) and 156 (29.9%) were negative for both serological tests. Only one person (0.2%) had negative SMP-ELISA and positive COPT (Figure 1).

Stool examination performed was positive almost on the same frequency in women (47.6%) than in men (52.4%). Significant differences regarding gender and age were not observed.

Immunodiagnostic accuracy

The comparison between SMP-ELISA and the presence of S. mansoni eggs in stools is shown in Table (2) and validity parameters results are summarized in Table (3). It was found that SMP-ELISA had 95.2% sensitivity, and 31.2% specificity. From the 378 persons with negative COPT only two (0.5%) had S. mansoni eggs (Table 2). The sensitivity of COPT was 90.5%, the specificity 75.2% (Table 3). PPV was low both for SMP-ELISA and COPT (5.5% and 13.3%, respectively) although NPV was high (above 99.0%) (Table 3). Positive likelihood ratios were quite low although they were higher for COPT (Table 3).

From the 364 people with positive SMP-ELISA (data not shown), 142 (39.0%) had simultaneously positive COPT and, from 157 persons with negative SMP-ELISA, only one (0.6%) had positive COPT (Figure 1). When simultaneous SMP-ELISA and COPT were used, net sensitivity was 99.6% and net specificity 23.2%. When sequential (two-stage) tests were achieved, net sensitivity was 86.2% and net specificity 82.2%.

Among 344 individuals with positive SMP-ELISA and without S. mansoni eggs, 203 (59.0%) had evidence of schistosomiasis in previous parasitological survey registers (1976-1989).

Table 1: Demographic characteristic and previous status of schistosomiasis infection and sickness of study population, Brejo do Espírito Santo, Bahia State, Brazil, 2002-2003.

Study population Participants (n) Gender Age (median and range) Previous schistosomiasis (1976-1989) Hepatic or hepatosplenic pathology attributable to S. mansoni
Male Female
General census 3164 1594 (50.4%) 1570 (46.6%) 28 (1-90) 1522 (41.1%) 354 (11.2%)
Sampling 521 268 (51.4%) 253 (48.6%) 28 (2-90) 284 (54.5%) 85 (16.3%)

Table 2: Comparison of serological tests for schistosomiasis and stool examination by the Kato-Katz method at Brejo do Espírito Santo, Bahia State, Brazil, 2002-2003.

Serological test (n) Kato-Katz method (n)
Positive Negative Total
SMP-ELISA Positive 20 344 364
Negative 1 156 157
Total 21 500 521
COPT Positive 19 124 143
Negative 2 376 378
Total 21 500 521

Table 3: Field validity parameters of the comparisons between SMP-ELISA, COPT with the Kato-Katz method as gold standard at Brejo do Espírito Santo, Bahia State, Brazil, 2002-2003. 

Serological tests under study Validity parameter
Sensitivity% (95%CI) Specificity% (95%CI) % (95%CI) NPV% (95%CI) PLR Ratio(95%CI) NLR Ratio(95%CI)
SMP-ELISA 95.2(74.1-99.8) 31.2(27.2-35.5) 5.5(3.5-8.5) 99.4(96.0-100) 1.4(1.2-1.6) 0.2(0-1.0)
COPT 90.5(68.1-98.3) 75.2(71.1-78.9) 13.3(8.4-20.2) 99.5(97.9-99.9) 3.7(3.0-4.5) 0.1(0-0.5)
Abbreviations: PPN: Positive Predictive Value; NPV: Negative Predictive Value; PLR: Positive Likelihood Ratio; NLR: Negative Likelihood Ratio: 95%CI: 95% Confidence Interval



When we performed this study, the situation of schistosomiasis in Brejo do Espírito Santo was of low endemicity, a condition diametrically opposed to that observed in 1976, when it was characterized as hiperendemic area before the implementation of control measures based on health education [27]. In the present study, the prevalence of schistosomiasis based on coprology was 1.8% and 31% by SMP-ELISA.

SMP-ELISA showed high sensitivity compared to a single stool examination which is the most common situation at endemic areas subject to control programs. SMP-ELISA was positive in 31% of the individuals surveyed, especially adults. However, it is likely that many of them were old cases of schistosomiasis that existed in the community when there was elevated transmission and which retain antibodies despite the parasitological cure. In fact, 59% of positive SMP-ELISA without S. mansoni eggs in stools had eggs of this helminth sometime during the period 1976- 1989. In spite of the high sensitivity, PPV was poor indicating the effect of low prevalence.

Likelihood ratios are estimated on sensitivity and specificity values and do not depend on the prevalence of the disease [34]. The low value of PLR does not qualify SMP-ELISA as an adequate technique to diagnose schistosomiasis. In contrast, its low NLR makes SMP-ELISA an excellent test to rule out the infection.

Likelihood ratios are estimated on sensitivity and specificity values and do not depend on the prevalence of the disease [34]. The low value of PLR does not qualify SMP-ELISA as an adequate technique to diagnose schistosomiasis. In contrast, its low NLR makes SMP-ELISA an excellent test to rule out the infection.

In this survey we confirmed that COPT hardly gives positive results when SMP-ELISA is negative; maybe, if we emphasize the search of S. mansoni eggs in those COPT positive persons we could recognize more people eliminating eggs in stools. In 124 individuals with positive COPT we cannot identify S. mansoni eggs (false negatives?). It is possible to explain these by method failure, or because the majority of eggs have been retained in the tissues, as suggested by Pugh [39], by the presence of fibrosis, which hinder the passage of eggs to the gut lumen. We must also consider the possibility that these patients might have longstanding infections with adult worms, with low fertility and decreased deposition of eggs [40]. The low intensity of infection may affect the sensitivity and specificity of serology [35] although Ruiz-Tiben et al. [41], disagree with this theory. The probability of unisexual infection does not explain this fact because in these circumstances COPT would also be negative [42].

Other possible explanations for false-negative results should be considered. It is more likely that operational conditions such as eventual failures in the storage and transportation of serum samples from the endemic area to Uberaba, and later to the reference laboratory in Venezuela may be responsible for these results. Lambertucci et al. [43], have described the possibility of false negatives of COPT due to loss of antibodies because of improper sample storage. Therefore, we propose a similar study using tests such as SMP-ELISA and COPT and increasing the number of Kato-Katz samples to assess the proportion of false negative in serology in schistosomiasis low transmission areas.

We found 0.4% (2/521) of patients with S. mansoni-eggs in stools with negative COPT, a finding similar to that obtained by Espírito Santo et al. [25], (0.2%); they also found that 1-1.8% of patients had negative ELISA-IgM or ELISA-IgG with positive COPT, we observed only 1 from 521 persons (0.2%) with negative SMPELISA and positive COPT, possibly explained by the use of SMP which reduces, but not eliminated cross reactivity with other trematodes and soil-transmitted helminths [31].

As a single, simple, sensitive, and specific assay for field diagnosis of schistosomiasis is not yet available [44], immunodiagnostic tests could be an alternative. However, the use of SMP-ELISA and COPT should be carefully weighted. The ideal situation would be the use of both serological tests simultaneously which increases the sensitivity as demonstrated by Ibrahim & Ibrahim [45] which also used combination use several test for diagnosis schistosomiasis in Central Sudan; in this case, they used, as well as the Kato-Katz method, ELISA and IHA and found good sensitivity (93.3%) and increased specificity to 85.8% and PPV to 55.1% with the simultaneous use of both serological techniques. Authors found at least 3/125 positive patients with positive Kato-Katz with negative ELISA and IHA. In thestudyconducted in Rio de Janeiro, Brazil, Espírito Santo et al. [25], suggest that the combination of these diagnostic tools could be useful for the diagnosis of schistosomiasis in epidemiological studies in areas of low endemicity.

Despite the fact that combined approaches have been successful in diagnostic screening, whereby individuals are initially tested for the presence of anti-schistosomal antibodies and then those with positive results confirmed by copro-microscopy techniques [29], the approach can be logistically demanding and time-consuming. On the other hand, if serodiagnosis is used alone, there is the likelihood of underestimating the true prevalence of infection because the majority of methods for determining antischistosomal antibodies tend to remain positive for several years and it is difficult to differentiate between an active infection and previous exposure to an infection that has been cleared [16], in addition, there is variable rates of cross-reactivity with other trematodes and soil-transmitted helminths, leading to lower test reproducibility and reduced specificity, and therefore to the impossibility to determine the intensity of infection [16].

As mentioned before, COPT is laborious and expensive to be performed limiting its use in the field at the present moment. On the other hand, the use of sequential tests would increase specificity decreasing the probability of false positives but it has the disadvantage of decreasing the capability of identifying true positives. In the present study, the probability of falsenegative results with sequential tests was approximately 14%. In face of these results, the decision of using sequential or simultaneous testing should be based on the objective [46]. In this case, the goal is the screening of population for control purposes. Therefore, COPT is unfeasible due to the high laboratory requirements. The ideal situation would be the use of simultaneous testing alternative for surveillance and control as well as for epidemiological studies in low endemic areas in which the whole community would be screened using SMP-ELISA and only those individuals who were positive, would be retested using COPT. SMP-ELISA is highly sensitive, easier, faster, and more economic. Confirmatory test (COPT) would increase the net specificity ruling out false positives. Often, treating those positive SMP-ELISA would result more cost-effective than repeating stool examination because of the low costs of praziquantel, although at endemic areas of cysticercosis it might be used with caution. Frota et al. [47], proposed to use ELISA with eggs antigens for screening populations, with subsequent diagnostic confirmation with Kato-Katz, In this study, the initial prevalence by the KatoKatz method (3.8%) increased to 8.7% when the feces exam was repeated oriented by positive results of ELISA; similarly, in a low endemic area in Ceará (Brazil), Pinheiro et al. [48], preselected individuals through the use of a serological technique like ELISA with adult worm antigen and, thereafter performed three combined parasitological methods for schistosomiasis diagnosis. Using Kato-Katz, 9.1% of fecal samples were positive for S. mansoni eggs, while the saline gradient method resulted in a detection of 18.2%, and 42.4% using the Helmintex® 48].

When prevalence of schistosomiasis and parasitic load are very low, the Kato-Katz method loses sensitivity. In this circumstances, even when the stool exam or slides are repeated several times (until 25 slides according to Ferrari et al. [49], the probability to find one S. mansoni egg is very low. Under field conditions, for control and sureillance purposes, health workers of the Brazilian Control Program routinely make only one slide per patient. In previous approaches since the 70´s in this hiper endemic community Prata et al. [50], and Ruiz-Guevara [27] estimated the prevalence using only one Kato-Katz slide and we considered appropriate to determine the prevalence in the same conditions after massive interventions. On the other hand, in low endemic areas the preparation of multiple slides and samples for each individual results in logistical difficulties, thus neutralizing the operational advantages of the technique [51]. Therefore, in schistosomiasis low endemic areas, it is important to use first techniques with elevated sensitivity as SMP-ELISA and then confirmation with more specific and laborious test as COPT.

As with other infectious diseases such as Chagas disease, AIDS, toxoplasmosis, where a sensitive laboratory test is used first, and afterward, another technique, more specific to define individuals who are actually infected, in areas of low prevalence of schistosomiasis, as is now the Brejo do Espírito Santo, it is fully justified the use of sequential tests to identify those people who require specific treatment. This can be a solution for evaluating schistosomiasis control programmes in Brazil. The difficulties or limitations of antibody persistence inherent to serology after cure, and the high proportion of false positives widely referred to in the literature [14], would be solved with the use of sequential testing, and would make the rapid immunodiagnostic methods, a useful tool to monitor the effects of treatment and other control measures. A new era in the diagnosis of schistosomiasis comes with the fall of parasitological detection as the gold-standard test in low transmission areas [52].


For epidemiological surveys we suggest the use of an easy, fast and cost-effective test as SMP-ELISA as initial screening method; the positives should be tested again with a specific confirmatory technique such as the COPT to identify real positives. Moreover, in those COPT positive persons, it might be useful to emphasize the search of S. mansoni eggs.


We would like to thank the staff of the 26th Regional Health Board (DIRES) de Santa Maria da Vitória, especially to Gercino José Nogueira, Eliezer GonçalvesAraújo, José Maria dos Santos, Diolirio Pereira da Silva, Adam José dos Santos for the stool examinations. The personnel of the Family Health Program of Brejo do Espírito Santo. Special thanks to Dr. Julio Castro for his kind contribution on the data analysis of this research and to Dr. Oscar Noyaand Dr. Carlos Mauricio de Figueiredo Antunes for their valuable comments on the manuscript. To the entire population of Brejo do Espírito Santo, for their kindness and cooperation for the realization of this work. Research funded by FAPEMIG.


1. Berhe N, Medhin G, Erko B, Smith T, Gedamu S, Bereded D, et al. Variations in helminth faecal egg counts in Kato-Katz thick smears and their implications in assessing infection status with Schistosoma mansoni. Acta Trop. 2004; 92: 205-212.

2. Kongs A, Marks G, Verlé P, Van der Stuyft P. The unreliability of the Kato-Katz technique limits its usefulness for evaluating S. mansoni infections. Trop Med Int Health. 2001; 6: 163-169.

3. de Vlas SJ, Gryseels B. Underestimation of Schistosoma mansoni prevalences. Parasitol Today. 1992; 8: 274-277.

4. Enk MJ, Lima AC, Drummond SC, Schall VT, Coelho PM. The effect of the number of stool samples on the observed prevalence and the infection intensity with Schistosoma mansoni among a population in an area of low transmission. Acta Trop. 2008; 108: 222-228.

5. World Health Organization. The control of schistosomiasis. WHO Technical Report Series. 1993.

6. Mc Carthy J, Lustigman S, Yang GJ, Barakat R, Garcia HH, Sripa B, et al. A research agenda for helminth diseases of humans: Diagnostics for control and elimination programmes. PLoS Negl Trop Dis. 2012; 6: e1601.

7. Burlandy-Soares LC, de Souza Dias LC, Kanamura HY, de Oliveira EJ, Ciaravolo RM. Schistosomiasis mansoni: follow-up of control program based on parasitologic and serologic methods in a Brazilian community of low endemicity. Mem Inst Oswaldo Cruz. 2003; 98: 853- 859.

8. Engels D, Sinzinkayo E, Gryseels B. Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. Am J Trop Med Hyg. 1996; 54: 319-324.

9. Feldmeier H, Poggensee G. Diagnostic techniques in schistosomiasis control. A review. Acta Trop. 1993; 52: 205-220.

10. Lin DD, Liu JX, Liu YM, Hu F, Zhang YY, Xu JM, et al. Routine Kato-Katz technique underestimates the prevalence of Schistosoma japonicum: a case study in an endemic area of the People’s Republic of China. Parasitol Int. 2008; 57: 281-286.

11. Utzinger J, Booth M, N’Goran EK, Muller I, Tanner M, Lengeler C. Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology. 2001; 122: 537-544.

12. World Health Organization. Schistosomiasis: Progress Report 2001- 2011 and Strategic Plan 2012-2020. WHO. 2013.

13. Passos AD, Amaral Rdos S. Schistosomiasis mansoni: the epidemiological and control aspects. Rev Soc Bras Med Trop. 1998; 31: 61-74.

14. World Health Organization. Report of the informal consultation on schistosomiasis in low transmission areas: Control strategies and criteria for elimination. 2011.

15. Zhou YB, Zheng HM, Jiang QW. A diagnostic challenge for schistosomiasis japonica in China: consequences on praziquantel based morbidity control. Parasit Vectors. 2011; 4: 194.

16. Weerakoon KG, Gobert GN, Cai P, Mc Manus DP. Advances in the Diagnosis of Human Schistosomiasis. Clin Microbiol Rev. 2015; 28: 939-967.

17. Gomes LI, Enk MJ, Rabello A. Diagnosing schistosomiasis: where are we? Rev Soc Bras Med Trop. 2014; 47: 3-11.

18. Van Lieshout L, Panday UG, De Jonge N, Krijger FW, Oostburg BF, Polderman AM, et al. Immunodiagnosis of schistosomiasis mansoni in a low endemic area in Surinam by determination of the circulating antigens CAA and CCA. Acta Trop. 1995; 59: 19-29.

19. Alarcón de Noya B, Ruiz R, Caracciolo MA, Hernán A, Losada S, Colmenares C, et al. Epidemiologic surveillance for schistosomiasis in endemic areas. Acta Cien Venez. 1998; 49: 297.

20. Alarcón de Noya B, Balzan C, Arteaga C, Cesari I, Noya O. The last fifteen years of schistosomiasis in Venezuela: features and evolution. Mem Inst Oswaldo Cruz. 1999; 94: 139-146.

21. Noya BA, Guevara RR, Colmenares C, Losada S, Noya O. Low transmission areas of schistosomiasis in Venezuela: consequences on the diagnosis, treatment, and control. Mem Inst Oswaldo Cruz. 2006; 101: 29-35.

22. Alarcón de Noya B, Ruiz R, Losada S, Colmenares C, Contreras R, Cesari IM, et al. Detection of schistosomiasis cases in low-transmission areas based on coprologic and serologic criteria The Venezuelan experience. Acta Trop. 2007; 103: 41-49.

23. Gonçalves MM, Barreto MG, Peralta RH, Gargioni C, Gonçalves T, Igreja RP, et al. Immunoassays as an auxiliary tool for the serodiagnosis of Schistosoma mansoni infection in individuals with low intensity of egg elimination. Acta Trop. 2006; 100: 24-30.

24. Noya O, Alarcón de Noya B, Losada S, Colmenares C, Guzmán C, Lorenzo MA, et al. Laboratory diagnosis of Schistosomiasis in areas of low transmission: a review of a line of research. Mem Inst Oswaldo Cruz. 2002; 97: 167-169.

25. Espirito-Santo MCC, Pinto PL, Gargioni C, Alvarado-Mora MV, Pagliusi-Cartilho VL, Pinho JR, et al. Detection of Schistosoma mansoni antibodies in a low endemicity area using indirect immunofluorescence and circumoval precipitin test. Am J Trop Med Hyg. 2014; 90: 1146-1152.

26. Guangjin S, Mingdao J, Qiyang L, Hui X, Jiangming H, Xiaomei Y. Study on histopathology, ultrasonography and some special serum enzymes and collagens for 38 advanced patients of schistosomiasis japonica. Acta Trop. 2002; 82: 235-246.

27. Ruiz-Guevara R. Esquistossomosena reahyperendmica of Brejo do Esp rito Santo, Bahia, with follow-up of 29 years. Thesis submitted to the Postgraduate Course in Tropical Medicine and Infectious Diseases at Federal University of Tri ngulo Mineiro for obtaining the degree of Doctor. 2005; 275.

28. Wu G. A historical perspective on the immuno diagnosis of schistosomiasis in China. Acta Trop. 2002; 82: 193-198.

29. Zhu YC. Immunodiagnosis and its role in schistosomiasis control in China: a review. Acta Trop. 2005; 96: 130-136.

30. Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1972; 14: 397-400.

31. Alarcon de Noya B, Colmenares C, Lanz H, Caracciolo MA, Losada S, Noya O. Schistosoma mansoni: Immunodiagnosis is improved by sodium metaperiodate which reduces cross-reactivity due to glycosylated epitopes of soluble egg antigen. Exp Parasitol. 2000; 95: 106-112.

32. Spencer L, Alarcón de Noya B, Noya O, Masroua G. Comparative analysis between the circumoval precipitin test and ELISA with raw antigens for the diagnosis of schistosomiasis in Venezuela. GEN. 1991; 45: 77-83.

33. Grimes DA, Schulz KF. Refining clinical diagnosis with likelihood ratios. Lancet. 2005; 365: 1500-1505.

34. Otero W, Pineda LF, Beltrn LH. Usefulness of likelihood ratio in the practical practice of comparability of likelihood ratio in clinical practice. Rev. Col. Gastroenterola. 2001; 16: 33-36.

35. Mott KE, Dixon H. Collaborative study on antigens for immunodiagnosis of schistosomiasis. Bull World Health Organ. 1982; 60: 729-753.

36. De Noya BA, Spencer L, Noya O. Pre- and post-treatment immunodiagnostic evaluation in human schistosomiasis mansoni. Mem Inst Oswaldo Cruz. 1992; 87: 271-276.

37. Hillyer GV, Soler de Galanes M. Seroepidemiology of schistosomiasis in Puerto Rico: evidence for vanishing endemicity. Am J Trop Med Hyg. 1999; 60: 827-830.

38. Rifat MA, Ismail I, el-Mahallawy MN, Awwaad S, Essawy M. A comparative study of some immunological tests for schistosomiasis before and after treatment. Trans R Soc Trop Med Hyg. 1969; 63: 338- 342.

39. Pugh RN. Periodicity of output of Schistosoma haematobium eggs in the urine. Ann Trop Med Parasitol. 1979; 73: 89-90.

40. Gryseels B. Human resistance to Schistosoma infection: age or experience? Parasitol Today. 1994; 10: 380-384.

41. Ruiz-Tiben E, Hillyer GV, Knight WB, Gómez de Rios I, Woodall JP. Intensity of infection with Schistosoma mansoni: its relationship to the sensitivity and specificity of serologic tests. Am J Trop Med Hyg. 1979; 28: 230-236.

42. Losada S, Siegert N, Matos C, Cesari IM, Alarc’n de Noya B. Immunological diagnosis of unisex infections by Schistosoma mansoni in mice. Acta Cien Venez. 1998; 49: 296.

43. Lambertucci JR, de Mello RT, Pedroso ER, Greco DB, Rocha MO. The circumoval precipitin test as a control of cure in children with chronic schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1983; 25: 37- 41.

44. Doenhoff MJ, Chiodini PL, Hamilton JV. Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends Parasitol. 2004; 20: 35-39.

45. Ibrahim AM, Ibrahim ME. Evaluation of microscopical and serological techniques in the diagnosis of Schistosoma mansoni infection at Sennar State, Central Sudan. Asian Pacific J Trop Dis. 2014; 4: 8-13.

46. Gordis L. Epidemiology. 5th Edn. Saunders Elsevier. 2014.

47. da Frota SM, Carneiro TR, Queiroz JA, Alencar LM, Heukelbach J, Bezerra FS. Combination of Kato-Katz faecal examinations and ELISA to improve accuracy of diagnosis of intestinal schistosomiasis in a low-endemic setting in Brazil. Acta Trop. 2011; 120: S138-141.

48. Pinheiro MC, Carneiro TR, Hanemann AL, Oliveira SM, Bezerra FS. The combination of three faecal parasitological methods to improve the diagnosis of schistosomiasis mansoni in a low endemic setting in the state of Ceará, Brazil. Mem Inst Oswaldo Cruz. 2012; 107: 873-876.

49. Ferrari ML, Coelho PM, Antunes CM, Tavares CA, da Cunha AS. Efficacy of oxamniquine and praziquantel in the treatment of Schistosoma mansoni infection: a controlled trial. Bull World Health Organ. 2003; 81: 190-196.

50. Prata A, Ruiz-Guevara R, Ricardo SA. Exceptional improvement of schistosomiasis: epidemiological pattern in anhyperendemic area. In: 9th Internacional Symposium on Schistosomiasis. 2003; 165.

51. Teles HM, Ferreira CS, de Carvalho ME, Zacharias F, Magalhães LA. The efficiency of the examination of compressed fecal samples for Schistosoma mansoni eggs. Rev Soc Bras Med Trop. 2003; 36: 503- 507.

52. Cavalcanti MG, Silva LF, Peralta RH, Barreto MG, Peralta JM. Schistosomiasis in areas of low endemicity: a new era in diagnosis. Trends Parasitol. 2013; 29: 75-82.

Received : 26 Oct 2016
Accepted : 22 Nov 2016
Published : 24 Nov 2016
Annals of Otolaryngology and Rhinology
ISSN : 2379-948X
Launched : 2014
JSM Schizophrenia
Launched : 2016
Journal of Nausea
Launched : 2020
JSM Internal Medicine
Launched : 2016
JSM Hepatitis
Launched : 2016
JSM Oro Facial Surgeries
ISSN : 2578-3211
Launched : 2016
Journal of Human Nutrition and Food Science
ISSN : 2333-6706
Launched : 2013
JSM Regenerative Medicine and Bioengineering
ISSN : 2379-0490
Launched : 2013
JSM Spine
ISSN : 2578-3181
Launched : 2016
Archives of Palliative Care
ISSN : 2573-1165
Launched : 2016
JSM Nutritional Disorders
ISSN : 2578-3203
Launched : 2017
Annals of Neurodegenerative Disorders
ISSN : 2476-2032
Launched : 2016
Journal of Fever
ISSN : 2641-7782
Launched : 2017
JSM Bone Marrow Research
ISSN : 2578-3351
Launched : 2016
JSM Mathematics and Statistics
ISSN : 2578-3173
Launched : 2014
Journal of Autoimmunity and Research
ISSN : 2573-1173
Launched : 2014
JSM Arthritis
ISSN : 2475-9155
Launched : 2016
JSM Head and Neck Cancer-Cases and Reviews
ISSN : 2573-1610
Launched : 2016
JSM General Surgery Cases and Images
ISSN : 2573-1564
Launched : 2016
JSM Anatomy and Physiology
ISSN : 2573-1262
Launched : 2016
JSM Dental Surgery
ISSN : 2573-1548
Launched : 2016
Annals of Emergency Surgery
ISSN : 2573-1017
Launched : 2016
Annals of Mens Health and Wellness
ISSN : 2641-7707
Launched : 2017
Journal of Preventive Medicine and Health Care
ISSN : 2576-0084
Launched : 2018
Journal of Chronic Diseases and Management
ISSN : 2573-1300
Launched : 2016
Annals of Vaccines and Immunization
ISSN : 2378-9379
Launched : 2014
JSM Heart Surgery Cases and Images
ISSN : 2578-3157
Launched : 2016
Annals of Reproductive Medicine and Treatment
ISSN : 2573-1092
Launched : 2016
JSM Brain Science
ISSN : 2573-1289
Launched : 2016
JSM Biomarkers
ISSN : 2578-3815
Launched : 2014
JSM Biology
ISSN : 2475-9392
Launched : 2016
Archives of Stem Cell and Research
ISSN : 2578-3580
Launched : 2014
Annals of Clinical and Medical Microbiology
ISSN : 2578-3629
Launched : 2014
JSM Pediatric Surgery
ISSN : 2578-3149
Launched : 2017
Journal of Memory Disorder and Rehabilitation
ISSN : 2578-319X
Launched : 2016
JSM Head and Face Medicine
ISSN : 2578-3793
Launched : 2016
JSM Cardiothoracic Surgery
ISSN : 2573-1297
Launched : 2016
JSM Bone and Joint Diseases
ISSN : 2578-3351
Launched : 2017
JSM Bioavailability and Bioequivalence
ISSN : 2641-7812
Launched : 2017
JSM Atherosclerosis
ISSN : 2573-1270
Launched : 2016
Journal of Genitourinary Disorders
ISSN : 2641-7790
Launched : 2017
Journal of Fractures and Sprains
ISSN : 2578-3831
Launched : 2016
Journal of Autism and Epilepsy
ISSN : 2641-7774
Launched : 2016
Annals of Marine Biology and Research
ISSN : 2573-105X
Launched : 2014
JSM Health Education & Primary Health Care
ISSN : 2578-3777
Launched : 2016
JSM Communication Disorders
ISSN : 2578-3807
Launched : 2016
Annals of Musculoskeletal Disorders
ISSN : 2578-3599
Launched : 2016
Annals of Virology and Research
ISSN : 2573-1122
Launched : 2014
JSM Renal Medicine
ISSN : 2573-1637
Launched : 2016
Journal of Muscle Health
ISSN : 2578-3823
Launched : 2016
JSM Genetics and Genomics
ISSN : 2334-1823
Launched : 2013
JSM Anxiety and Depression
ISSN : 2475-9139
Launched : 2016
Clinical Journal of Heart Diseases
ISSN : 2641-7766
Launched : 2016
Annals of Medicinal Chemistry and Research
ISSN : 2378-9336
Launched : 2014
JSM Pain and Management
ISSN : 2578-3378
Launched : 2016
JSM Women's Health
ISSN : 2578-3696
Launched : 2016
Clinical Research in HIV or AIDS
ISSN : 2374-0094
Launched : 2013
Journal of Endocrinology, Diabetes and Obesity
ISSN : 2333-6692
Launched : 2013
Journal of Substance Abuse and Alcoholism
ISSN : 2373-9363
Launched : 2013
JSM Neurosurgery and Spine
ISSN : 2373-9479
Launched : 2013
Journal of Liver and Clinical Research
ISSN : 2379-0830
Launched : 2014
Journal of Drug Design and Research
ISSN : 2379-089X
Launched : 2014
JSM Clinical Oncology and Research
ISSN : 2373-938X
Launched : 2013
JSM Bioinformatics, Genomics and Proteomics
ISSN : 2576-1102
Launched : 2014
JSM Chemistry
ISSN : 2334-1831
Launched : 2013
Journal of Trauma and Care
ISSN : 2573-1246
Launched : 2014
JSM Surgical Oncology and Research
ISSN : 2578-3688
Launched : 2016
Annals of Food Processing and Preservation
ISSN : 2573-1033
Launched : 2016
Journal of Radiology and Radiation Therapy
ISSN : 2333-7095
Launched : 2013
JSM Physical Medicine and Rehabilitation
ISSN : 2578-3572
Launched : 2016
Annals of Clinical Pathology
ISSN : 2373-9282
Launched : 2013
Annals of Cardiovascular Diseases
ISSN : 2641-7731
Launched : 2016
Journal of Behavior
ISSN : 2576-0076
Launched : 2016
Annals of Clinical and Experimental Metabolism
ISSN : 2572-2492
Launched : 2016
Clinical Research in Infectious Diseases
ISSN : 2379-0636
Launched : 2013
JSM Microbiology
ISSN : 2333-6455
Launched : 2013
Journal of Urology and Research
ISSN : 2379-951X
Launched : 2014
Journal of Family Medicine and Community Health
ISSN : 2379-0547
Launched : 2013
Annals of Pregnancy and Care
ISSN : 2578-336X
Launched : 2017
JSM Cell and Developmental Biology
ISSN : 2379-061X
Launched : 2013
Annals of Aquaculture and Research
ISSN : 2379-0881
Launched : 2014
Clinical Research in Pulmonology
ISSN : 2333-6625
Launched : 2013
Journal of Immunology and Clinical Research
ISSN : 2333-6714
Launched : 2013
Annals of Forensic Research and Analysis
ISSN : 2378-9476
Launched : 2014
JSM Biochemistry and Molecular Biology
ISSN : 2333-7109
Launched : 2013
Annals of Breast Cancer Research
ISSN : 2641-7685
Launched : 2016
Annals of Gerontology and Geriatric Research
ISSN : 2378-9409
Launched : 2014
Journal of Sleep Medicine and Disorders
ISSN : 2379-0822
Launched : 2014
JSM Burns and Trauma
ISSN : 2475-9406
Launched : 2016
Chemical Engineering and Process Techniques
ISSN : 2333-6633
Launched : 2013
Annals of Clinical Cytology and Pathology
ISSN : 2475-9430
Launched : 2014
JSM Allergy and Asthma
ISSN : 2573-1254
Launched : 2016
Journal of Neurological Disorders and Stroke
ISSN : 2334-2307
Launched : 2013
Annals of Sports Medicine and Research
ISSN : 2379-0571
Launched : 2014
JSM Sexual Medicine
ISSN : 2578-3718
Launched : 2016
Annals of Vascular Medicine and Research
ISSN : 2378-9344
Launched : 2014
JSM Biotechnology and Biomedical Engineering
ISSN : 2333-7117
Launched : 2013
Journal of Hematology and Transfusion
ISSN : 2333-6684
Launched : 2013
JSM Environmental Science and Ecology
ISSN : 2333-7141
Launched : 2013
Journal of Cardiology and Clinical Research
ISSN : 2333-6676
Launched : 2013
JSM Nanotechnology and Nanomedicine
ISSN : 2334-1815
Launched : 2013
Journal of Ear, Nose and Throat Disorders
ISSN : 2475-9473
Launched : 2016
JSM Ophthalmology
ISSN : 2333-6447
Launched : 2013
Journal of Pharmacology and Clinical Toxicology
ISSN : 2333-7079
Launched : 2013
Annals of Psychiatry and Mental Health
ISSN : 2374-0124
Launched : 2013
Medical Journal of Obstetrics and Gynecology
ISSN : 2333-6439
Launched : 2013
Annals of Pediatrics and Child Health
ISSN : 2373-9312
Launched : 2013
JSM Clinical Pharmaceutics
ISSN : 2379-9498
Launched : 2014
JSM Foot and Ankle
ISSN : 2475-9112
Launched : 2016
JSM Alzheimer's Disease and Related Dementia
ISSN : 2378-9565
Launched : 2014
Journal of Addiction Medicine and Therapy
ISSN : 2333-665X
Launched : 2013
Journal of Veterinary Medicine and Research
ISSN : 2378-931X
Launched : 2013
Annals of Public Health and Research
ISSN : 2378-9328
Launched : 2014
Annals of Orthopedics and Rheumatology
ISSN : 2373-9290
Launched : 2013
Journal of Clinical Nephrology and Research
ISSN : 2379-0652
Launched : 2014
Annals of Community Medicine and Practice
ISSN : 2475-9465
Launched : 2014
Annals of Biometrics and Biostatistics
ISSN : 2374-0116
Launched : 2013
JSM Clinical Case Reports
ISSN : 2373-9819
Launched : 2013
Journal of Cancer Biology and Research
ISSN : 2373-9436
Launched : 2013
Journal of Surgery and Transplantation Science
ISSN : 2379-0911
Launched : 2013
Journal of Dermatology and Clinical Research
ISSN : 2373-9371
Launched : 2013
JSM Gastroenterology and Hepatology
ISSN : 2373-9487
Launched : 2013
Annals of Nursing and Practice
ISSN : 2379-9501
Launched : 2014
JSM Dentistry
ISSN : 2333-7133
Launched : 2013
Author Information X