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FIELD COMPARISON OF IMMUNODIAGNOSTIC AND PARASITOLOGICAL TECHNIQUES FOR THE DETECTION OF SCHISTOSOMIASIS JAPONICA IN THE PEOPLE’S REPUBLIC OF CHINA

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  • 1 Department of Epidemiology, School of Public Health, Fudan University, Shanghai, People’s Republic of China; Xuhui Center for Disease Control and Prevent, Shanghai, People’s Republic of China; Anhui Provincial Institute of Parasitic Diseases, Wuhu, People’s Republic of China; Key Laboratory of Public Health Safety, Fudan University, Ministry of Education, People’s Republic of China

A total of 1,811 individuals from two villages located in the areas of China endemic for Schistosoma japonicum were analyzed by the Kato-Katz parasitologic examination, indirect hemagglutination assay (IHA), and enzyme-linked immunosorbent assay (ELISA). Statistical analysis of the results showed the κ indices ranged from 0.106 to 0.234 between IHA and the stool examination and ranged from 0.037 to 0.134 between ELISA and the fecal examination. The sensitivity value of the IHA was 83.7% in Village A and 92.3% in Village B; the specificity value of the IHA was 55.8% in Village A and 67.3% in Village B. The sensitivity value of the ELISA was 88.4% in Village A and 96.2% in Village B; the specificity value of the ELISA was 38.4% in both Village A and Village B. A search for a good diagnostic test that can be applied in field situations in China should be given high priority.

INTRODUCTION

Schistosomiasis japonicum is one of the most serious public health problems in China, with a documented history of > 2,100 years. By the end of 2003, an estimated 843,011 people were infected with S. japonicum.1 At present, selective chemotherapy with the highly efficacious antischistosomal drug praziquentel is the main strategy for control of schistosomiasis in the national schistosomiasis program, because the prevalence and the morbidity of the disease are low after many years of mass chemotherapy, which was introduced in the early 1980s.2,3 Thus, diagnosis is a key step for the control of schistosomiasis.4 Determination of target populations for chemotherapy in the endemic communities, assessment of morbidity, and the evaluation of control strategies all build on the results from diagnostic tests.

Schistosomiasis diagnosis can be divided into direct parasitologic techniques (parasite eggs detection) and indirect approaches (detection of antibodies or circulating antigens in serum). Direct parasitologic techniques include standard tests of fecal examination using the Kato-Katz thick smear,5 which is currently the recommended method for diagnosing this disease,6 and the miracidium hatching test.7 Immunodiagnostic techniques include intradermal test (ID), circumoval precipitin test (COPT), indirect hemagglutination assay (IHA), enzyme-linked immunosorbent assay (ELISA), dipstick dye immunoassay (DDIA), and so on.8 IHA is currently the most widely used immunodiagnosis assay in the schistosomiasis-endemic areas of China for the demonstration of antibodies against schistosomiasis, whereas ELISA has become more important over the past 10–20 years. This paper presents the results of an extensive field comparison between the parasitologic Kato-Katz technique and IHA or ELISA in the two administrative villages of different intensities of S. japonicum infection.

MATERIALS AND METHODS

Study population.

A total of 1,055 persons from an administrative village (Village A) located in Jiangxi Province, China, and 859 individuals from another administrative village (Village B) located in Anhui Province, China, participated in this study. All residents were invited to participate in the study. These two villages are the areas endemic for infection with S. japonicum and were selected based on the previous known prevalence of the locality (Village A > 10% and Village B < 5%).9 Village A was composed of 49.7% women and 50.3% men, with an age range of 5–75 years (mean age = 36.4 years), and Village B was composed of 57.7% women and 42.3% men, with an age range of 5–75 years (mean age = 37.4 years).

Written informed consent was obtained from all adult participants and from the parents or legal guardians of minor. Ethical approval for the study was obtained from village (local government), country (anti-schistosomal), and provincial (schistosomiasis headquarters) authorities and was endorsed by the Jiangxi Provincial Institute of Parasitic Diseases and the Anhui Provincial Institute of Parasitic Diseases, respectively.

Fecal and blood samples.

For the population study, every inhabitant was asked to produce two stool specimens in 3 consecutive days. Every fecal specimen weight of 50 grams was analyzed by the Kato-Katz stool examination (three slides). During collection of stool samples, samples of 250 μL of finger tip blood were also collected for all participants in the study using the heparinized plastic capillary tubes, sealed at one end. These blood samples, as well as the fecal samples, were taken to local schistosomiasis stations, where IHA, ELISA and Kato-Katz tests were performed by laboratory staff within 24 hours of sample collection.

Stool examinations.

Fecal samples were evaluated for the presence of S. japonicum eggs by the quantitative Kato-katz thick smear parasitologic method.5 The stool examination was based on three slides (41.7 mg/smear) prepared from a single stool specimen, resulting in a total sample weight of 125 mg. Slides were read 1–12 hours after their initial preparation by two experienced technicians who were unaware of the subject’s medical status or immunologic test result. S. japonicum egg counts were expressed in eggs per gram of stool (epg), using the arithmetic mean of egg counts obtained from six slides (a total of six slides from two stool specimens), multiplied by 24. These individuals with a positive stool examination result were treated with a single oral dose of prazi-quantel (40 mg/kg).

Immunodiagnostic assay.

Each serum sample in the study was detected with IHA and ELISA. Sera were obtained by immediate separation by centrifugation after the blood samples were taken to local schistosomiasis stations. S. japonicum soluble egg antigen (SEA) was used as an antigen in the assay, and it was prepared according to a previous study.10 In brief, eggs of S. japonicum were collected from infected rabbit livers and were purified. Eggs were transferred in a 0.9% NaCl solution and homogenized for 1 hour on ice. The supernatants were collected after centrifugation at 20,000 rpm at 4°C to be the antigen (i.e., SEA).

The IHA test was carried out according to Wu and others.11 An IHA test kit was provided by the Anhui Provincial Institute of Parasitic Diseases. In brief, 100 μL of normal saline was placed into the first well of the transverse line, whereas 25 μL was placed into Wells 2 and 3. Then, 25 μL of serum was added to the first well and thoroughly mixed. In a subsequent step, 25 μL of this solution was added to the second well and mixed as before. The same procedure was repeated for the third well. Hence, the concentrations in the second and third wells were 1:10 and 1:20, respectively. Known positive and negative control sera were tested simultaneously on each plate.

We adhered to the following procedure. One drop of 2.5% sensitized red blood cell was placed into each well, shaken, and kept at room temperature for 1 hour. Observations were made by the naked eye. The highest titer where agglutination still appeared was regarded as the terminal point of a positive reaction. If a positive reaction appeared at a titer ≥ 1:10, the serologic test was considered positive.

The ELISA test was carried out according to a standard procedure.12 In brief, an Embed 96-well reaction plate with 100 μL of 1:700 diluted S. japonicum SEA was stored overnight. All sera were diluted 1/100 in 0.5% Tween-20 in phosphate-buffered saline (PBS) with 2% bovine serum albumin (BSA) before testing. The following control sera were used on each plate: a reference positive serum (serum from a patient with microscopically confirmed S. japonicum infection) and a tropical negative serum (serum from an individual with no evidence of S. japonicum infection from non-endemic area).

Aliquots of 100 μL of each diluted serum sample were dispensed into double wells on the plate. The plates were covered and incubated at 37°C for 30 minutes. After incubation, the plates were washed four times in wash solution. After washings, a 1/30,000 dilution of peroxidase-conjugated anti-human IgG was added to each well and incubated for 30 minutes at 37°C. After another series of washings, a chromogenic mixture of H2O2 and OPD (o-phenylenediamine), was added. After 10 minutes in the dark at 37°C and addition of stop solution (2 mol/L H2SO4), the optical density (OD) was measured with a Zs-3 microplate reader (China-Aerospace Science and Industry Corp., Beijing, China) at a wavelength of 450 nm. According to the manufacturer’s instructions, positive and negative control sera were measured simultaneously. In cases where the average OD value of double wells was 2.1-fold higher than that of the negative control sera, it was regarded as a positive reaction.

Statistical analysis.

Only data from subjects who agreed to all three tests were used for the analyses. To determine the detection rate of immunodiagnostic and parasitologic methods for different intensities of infection, individual arithmetic mean egg outputs over both surveys were classified into four eggs per gram categories: negative, light (1–100 epg), moderate (101–400 epg), and heavy (> 400 epg) infections. The comparative analysis for the performance of the different diagnostic methods, calculating sensitivity, specificity, and κ indices, was done using the SPSS Statistical Package for Social Sciences (SPSS, Chicago, IL). The χ2 for trend was done using the statistical package of EPI-INFO 6.04 version.13

RESULTS

A total of 1,024 cases in Village A had complete data, and the 31 individuals with missing values were excluded from our analyses. In Village B, there were 787 individuals with complete data, and 72 were excluded because of missing data. A total of 1,024 individuals were made up of 50.3% women and 49.7% men, with an age range of 5–75 years (mean age = 36.2 years), and 787 residents from Village B were made up of 58.8% women and 41.2% men, with an age range of 5–75 years (mean age = 37.6 years).

The prevalence of S. japonicum infection, calculated with the first and second Kato-Katz examination (three slides), was 12.7% (130/1,024) and 13.0% (133/1,024), respectively, in Village A and 4.6% (36/787) and 3.9% (31/787), respectively, in Village B. The prevalence determined with the first stool examination was not different significantly from that observed using the second stool examination in Village A (χ2 = 0.769, P > 0.05) and Village B (χ2 = 0.676, P > 0.05). Comparison of results obtained by the two stool examinations is shown in Table 1. Statistical analysis showed a κ index of 0.490 in Village A and 0.423 in Village B, indicating weak agreement between the two stool examinations.

Comparison of results obtained by the two accumulated and the single stool examinations is shown in Table 2. The positive cases of the two accumulated fecal examinations were these who had at last one positive count in the first or second stool examination, and the negative cases of the two accumulated fecal examinations were only those who had one negative count in both the first and second stool examination. The prevalence of S. japonicum infection, calculated with the two accumulated stool examinations, was 18.6% (190/1024) in Village A and 6.6% (52/787) in Village B. Assuming the two accumulated Kato-Katz results as the reference gold standard, the sensitivity of a single stool examination with the three-slide Kato-Katz method was 68.4% or 70.0% in Village A and 69.2% or 59.6% in Village B, respectively. Statistical analysis showed the κ indices ranged from 0.734 to 0.808, indicating good agreement between the two accumulated and the single stool examination.

Comparison of results obtained by the IHA and the stool examinations is shown in Table 3. Statistical analysis showed the κ indices ranged from 0.106 to 0.234, indicating very poor agreement between the two methods. Assuming the two accumulated Kato-Katz results as the reference gold standard, the sensitivity value of the IHA was 83.7% (159/190) in Village A and 92.3% (48/52) in Village B, and they were no significant differences (χ2 = 2.454, P > 0.05). The specificity value of the IHA was 55.8% (465/834) in Village A, which was lower (χ2 = 22.104, P < 0.01) than 67.3% (495/735) in Village B.

Based on individual arithmetic mean egg outputs over both surveys, the residents were classified into four egg per gram groups. The data in Table 4 show the positivity proportions determined with IHA in different intensities of infection. These positive proportion increased significantly (χ2trend = 87.873, P < 0.01 in Village A; χ2trend = 71.779, P < 0.01 in Village B) as the intensity of infection rose. Among the negative individuals determined with the Kato-Katz technique, the positive proportion determined with IHA was 44.2% in Village A and 32.7% in Village B.

Comparison of results obtained by ELISA and fecal examinations is shown in Table 5. Statistical analysis showed the κ indices ranged from 0.037 to 0.134, indicating very poor agreement between the two methods. Assuming the two accumulated Kato-Katz results as the reference gold standard, the sensitivity value of the ELISA was 88.4% (168/190) in Village A and 96.2% (50/52) in Village B, and there were no significant differences (χ2 = 2.732, P > 0.05). The specificity value of the ELISA was 38.4% (320/834) in Village A, which was the same (χ2 = 0.000, P > 0.05; 38.4%; 282/735) as Village B.

The data in Table 6 show the positivity proportions determined with ELISA in different intensities of infection. These positive proportion also rose significantly (χ2trend = 44.309, P < 0.01 in Village A; χ2trend = 24.133, P < 0.01 in Village B) as the intensity of infection grew. Among the negative individuals determined with the Kato-Katz technique, the positive proportion determined with ELISA was 61.6% in both Village A and Village B.

DISCUSSION

The availability of praziquantel, large-scale chemotherapy has been recognized to be a main approach for the control of S. japonicum over the past two decades in China, which resulted in the reduction of both prevalence and intensity of this infection year after year. Because reinfection is very common, especially in endemic areas of S. japonicum like China, the “test-treat” approach is probably the most cost-effective strategy to meet the needs of identifying target individuals for repeated retreatment. The parasitologic Kato-Katz technique, apart from being labor-intensive, time-consuming, and somewhat messy, has become relatively insensitive after widespread chemotherapy. Against this background, immunodiagnostic technology, because of its rapid, affordable, and easily acceptable (high compliance) advantages over parasitologic techniques, has been extensively, to a certain extent, indiscriminately adapted in the control program of schistosomiasis to identify the target persons for treatment.14 In this study, assuming the two accumulated Kato-Katz results as the reference gold standard, the sensitivity of a single stool examination with the three-slide Kato-Katz method was ~68.4–70.0% in Village A and ~59.6–69.2% in Village B. If the accumulated results of three or more repeated measurements were taken as the reference gold standard, the sensitivity of this single stool examination would be lower.15 The statistical agreement found between the two stool examinations was relatively low (κ < 0.50), showing the weak time-reliability of the Kato-Katz technique; this was mostly because of variation in fecal egg counts.15 Among positive persons observed with the two accumulated stool examinations, about one third of individuals who were positive in one stool examination were negative in another stool examination within 3 consecutive days. These people might be missed for treatment with prazi-quantel and continue to transmit S. japonicum.

The statistical agreement between the stool examination and IHA or ELISA was very weak (κ < 0.25), especially between the fecal examination and ELISA (κ < 0.15), showing very poor diagnostic agreement between the stool examination (the Kato-Katz technique) and the immunodiagnostic assay (IHA and ELISA) at an individual level. When the two accumulated Kato-Katz results were used as the “golden standard,” the sensitivity values of IHA and ELSA were high (> 83%), especially in areas of low endemicity; however, their specificity was very low (IHA: 55.8% in Village A, 67.3% in Village B; ELISA: 38.4% in Village A and B). These showed that the false-positive rates of IHA and ELISA were very high in field settings to identify villagers infected with S. japonicim. In some studies evaluating immunodiagnostic assays (IHA or ELISA), the false-positive rate of IHA was from 0% to 3.0% and that of ELISA was from 1.3% to 3.3%.8,14,16,17 These results were much lower than our field results (IHA: 44.2% in Village A, 32.7% in Village B; ELISA: 61.6% in both Village A and B). This is because of the serum samples from individuals living in schistosomiasis-free areas designated as normal controls in these studies of immunodiagnostic assays. However, the false seropositivity could be observed in a very high proportion of individuals classified into the negative group by stool examination in endemic areas, especially in areas with severe endemicity. In our experience in Village A, with relatively high intensity of infection, we found that the false-positive rate of IHA was 44.2% and that of ELISA was more (61.6%). The rates of seroprevalence of S. japonicum were 3–9 times higher than rates of prevalence determined by two repeated stool examinations and 4–16 times higher than rates of prevalence observed with a single fecal examination.

Theoretically, these false positivities of antibody-based immunodiagnostic assays might be composed of three groups: 1) patients infected with S. japonicum are misdiagnosed with stool examination; 2) cases with previous infection with S. japonicum are cured currently after effective treatment; 3) cases are infected with other parasites that are cross-reactive with S. japnicum. In our study, we made two repeated stool examinations with the Kato-Katz method in 3 consecutive days; therefore, the proportion of all infections misdiagnosed by two repeated measurements was relatively low, and these misdiagnoses were lightly infected individuals.15 These immunodiagnostic assays (IHA and ELISA) also missed a certain number of lightly infected individuals, especially in the areas of relatively severe endemicity. In Village A with relatively severe endemicity, the proportion of those lightly infected individuals that were misdiagnosed by IHA or ELISA was relatively high (18.2% [28/154] by IHA and 13.0% [20/154] by ELISA). Therefore, high false positives were not caused mainly by the low sensitivity of the Kato-Katz method. Wen and others18 reported that the cross-reactivities for detection of anti-S. japonicum antibody in sera obtained from patients with either paragonimiasis, hookworms, or A. lumbricoides by IHA and ELISA were 4.1% and 5.5%, respectively, and their IHA and ELISA methods are the same as our IHA and ELISA methods. Therefore, cross-reactivities with other parasites also could not cause the high false positives of antibody-based immunodiagnostic assays. In China, the immunodiagnostic assays (i.e., IHA and ELISA) have been used for screening target populations for selective chemotherapy on a large scale in schistosome-endemic areas at a prevalence of < 20%. In the case of immunologic assay being positive, the person in question is considered a suspected case of S. japoni-cum infection, and hence praziquantel is given.8 Reinfection is very common in endemic areas of S. japonicum and the anti-S. japonicum antibody will last > 1 year after effective treatment with preziquantel. Hence, such yearly chemotherapy with praziquantel on a large scale includes a large number of cases with positivity of anti-S. japonicum antibody but that are cured currently after effective treatment in the areas of relatively severe endemicity (such as Village A). Therefore, high false positives were caused mainly by the antibody-based immunodiagnostic assays (IHA and ELISA) not distinguishing active infection from previous infection or reinfection.

We are currently in a diagnostic dilemma with S. japonicum. The direct parasitologic techniques have become relatively insensitive after widespread chemotherapy that resulted in generally lower worm burdens, which leads to less efficiency in areas of low endemicity, in post-treatment situations, and in the control of transmission.14,19 Other diagnostic alternatives include immunologic methods, such as detection of antibodies or circulating antigens in serum. Antibody detection assays with high sensitivity but generally low specificity do not allow discrimination between active and previous infection or reinfection, which results in the difficulties in determining prevalence, identifying true infected individuals for selective chemotherapy, and assessing the effectiveness of intervention including follow-up of chemotherapy. The detection of circulating antigens is a highly specific assay but has not been shown to be more sensitive than the detection of eggs in areas of low endemicity.14,2023 Therefore, it is very difficult to select the diagnostic method for S. japonicum in areas with relatively severe endemicity (such as Village A). On one hand, if every person with a positive antibody-based immunodiagnostic assay is treated with praziquantel year after year, a considerable number of previous infections will be treated repeatedly, which results in abuse of praziquantel and reduction of chemotherapy compliance. On the other hand, if these immunodiagnostic assays are only used for preliminary screening, and all those with positive results are subjected to fecal examination to confirm infection, only residents with positive egg counts are treated, and a higher proportion of infections will be missed. Therefore, a search for a good diagnostic test that can be applied in field situations in China is essential and should be given high priority.

Table 1

Comparison of the two Kato-katz stool examinations (three slides) for the diagnosis of S. japonicum in the two villages

First stool examination
Second stool examinationNegativePositiveTotal
Village A
    Negative83457891
    Positive6073133
    Total8941301,024
κ index = 0.490
Village B
    Negative73521756
    Positive161531
    Total75136787
    κ index = 0.423
Table 2

Comparison of the two accumulated stool examinations and the single stool examination (three slides) for the diagnosis of S. japonicum in the two villages

Two accumulated stool examinations
NegativePositiveTotal
Village A
    First stool examination
        Negative83460894
        Positive0130130
        Total8341901,024
κ index = 0.792
    Second stool examination
        Negative83457891
        Positive0133133
        Total8341901,024
κ index = 0.779
Village B
    First stool examination
        Negative73516751
        Positive03636
        Total73552787
κ index = 0.808
    Second stool examination
        Negative73521756
        Positive03131
        Total73552787
κ index = 0.734
Table 3

Comparison of the IHA and the Kato-katz stool examinations (three slides) for the diagnosis of S. japonicum in the two villages

IHA
NegativePositiveTotal
Village A
    First stool examination
        Negative476418894
        Positive20110130
        Total4965281,024
κ index = 0.164
    Second stool examination
        Negative480411891
        Positive16117133
        Total4965281,024
κ index = 0.185
    Two accumulated stool examinations
        Negative465369834
        Positive31159190
        Total4965281,024
κ index = 0.234
Village B
    First stool examination
        Negative497254751
        Positive23436
        Total499288787
κ index = 0.140
    Second stool examination
        Negative495261756
        Positive42731
        Total499288787
κ index = 0.106
    Two accumulated stool examinations
        Negative495240735
        Positive44852
        Total499288787
κ index = 0.192
Table 4

Detection results obtained using the IHA method for different intensities of S. japonicum infection

IHA
GroupNumberNegativePositivePositivity rate (%)
Village A
    Negative83446536944.2
    Light infection1542812681.8
    Moderate infection2632388.5
    Heavy infection10010100.0
Village B
    Negative73549524032.7
    Light infection4944591.8
    Moderate infection303100.0
Table 5

Comparison of the ELISA and the Kato-katz stool examinations (three slides) for the diagnosis of S. japonicum in the two villages

ELISA
NegativePositiveTotal
Village A
    First stool examination
        Negative326568894
        Positive16114130
        Total3426821,024
κ index = 0.086
    Second stool examination
        Negative333558891
        Positive9124133
        Total3426821,024
κ index = 0.111
    Two accumulated stool examinations
        Negative320514834
        Positive22168190
        Total3426821,024
κ index = 0.134
Village B
    First stool examination
        Negative283468751
        Positive13536
        Total284503787
κ index = 0.049
    Second stool examination
        Negative282474756
        Positive22931
        Total284503787
κ index = 0.037
    Two accumulated stool examinations
        Negative282453735
        Positive25052
        Total284503787
κ index = 0.069
Table 6

Detection results obtained using the ELISA method for different intensities of S. japonicum infection

ELISA
GroupNumberNegativePositivePositivity rate (%)
Village A
    Negative83432051461.6
    Light infection1542013487.0
    Moderate infection2612596.2
    Heavy infection101990.0
Village B
    Negative73528245361.6
    Light infection4924795.9
    Moderate infection303100.0

*

Address correspondence to Qing-Wu Jiang, Department of Epidemiology, School of Public Health, Fudan University, Yixueyuan Road, Shanghai 200032, People’s Republic of China. E-mail: jiangqw@shmu.edu.cn

Authors’ addresses: Yi-biao Zhou, Genming Zhao, Jian-guo Wei, Wen-xiang Peng, and Qing-wu Jiang, Department of Epidemiology, School of Public Health, Fudan University, Yixueyuan Road, Shanghai 200032, People’s Republic of China, Telephone: 86-021-54237216, Fax: 86-021-64037350 and Key Laboratory of Public Health Safety, Fudan University, Ministry of Education, People’s Republic of China. Meixia Yang, Xuhui Center for Disease Control and Prevent, Jianguxi Road, Shanghai 200003, People’s Republic of China, Telephone: 86-021-64741079, Fax: 86-021-64741079. Qi-Zhi Wang, Anhui Provincial Institute of Parasitic Diseases, Wuhu 241100, People’s Republic of China, Telephone: 86-0553-3813983, Fax: 86-021-3822676.

Acknowledgments: The authors thank Tao Po and Chen Gen-xin for excellent assistance.

Financial support: This work was supported by National Natural Science Foundation of China (30590374) and The National High Technology Research and Development Program of China (2006AA02Z402).

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Author Notes

Reprint requests: Zhou Yi-biao, Department of Epidemiology, School of Public Health, Fudan University, Yixueyuan Road, Shanghai 200032, People’s Republic of China. E-mail: z_yibiao@hotmail.com.
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