|Year : 2016 | Volume
| Issue : 2 | Page : 95-102
Accuracy of immunochromatography diagnostic test versus microscopy in the diagnosis of malaria among clinically suspected patients in Jazan area, KSA
Wafaa M Zaki1, Aymen M Madkhali2
1 Department of Parasitology, Faculty of Medicine, Suez Canal University, Ismailia, Egypt; Medical Laboratory Technology Department, College of Applied Medical Sciences, Jazan University, Jazan, Kingdom of Saudi Arabia
2 Medical Laboratory Technology Department, College of Applied Medical Sciences, Jazan University, Jazan, Kingdom of Saudi Arabia
|Date of Submission||11-Jun-2016|
|Date of Acceptance||31-Oct-2016|
|Date of Web Publication||25-Apr-2017|
Wafaa M Zaki
Department of Parasitology, Faculty of Medicine, Suez Canal University, Ismailia, Egypt; Medical Laboratory Technology Department, College of Applied Medical Sciences, Jazan University, Jazan, Kingdom of Saudi Arabia
Source of Support: None, Conflict of Interest: None
Background Malaria has been documented as a major health problem in Saudi Arabia, and it is highly endemic especially in the Southwest (Jazan and Asir). Its control is considered a challenge; hence proper diagnosis is essential for implementation of successful control programs. Accordingly, the diagnostic test used should be easy, rapid, and reliable, besides it must be accurate and cost effective.
Objective This work aims to study reliability and diagnostic accuracy of an immunochromatographic test (ICT) using BinaxNOW® malaria test compared to microscopical examination of blood film as gold standard for malaria diagnosis among clinically suspected patients in Jazan area, KSA.
Methods A cross sectional prospective designed study was done for 200 patients with prolonged fever attending Jazan general hospitals. Venous blood samples were collected for both microscopic examination of Giemsa-stained thick and thin blood and rapid ICT (BinaxNOW®).
Results Microscopic examination of Giemsa-stained blood smears revealed 64 out of 200 cases (32%) positive for Plasmodium spp.; 43 out of 64 (67.2%) were positive for P. falciparum; 12 (18.7%) had mixed infection including P. falciparum; and 9 (14.1%) belonged to other Plasmodium spp. of which 8 (12.5%) were P. vivax and one case (1.6%) was P. ovale. ICT showed 66 out of 200 (33%) cases with positive results for Plasmodium spp. and one sample gave an invalid result. The overall sensitivity and specificity of ICT were 97% and 96%, respectively. While for single P. falciparum infection sensitivity and specificity were 96.7% and 78%, respectively. Regarding Plasmodium spp. other than P. falciparum sensitivity was 91.6% and specificity was 100%.
Conclusion The use of ICT complement to microscopy is of great value particularly in Jazan, KSA, where P. falciparum and P. vivax are the most prevalent Plasmodium spp. These methods help in expanding laboratory based diagnosis, and minimize malaria associated morbidity and mortality.
Keywords: BinaxNOW® malaria test, ICT, Jazan, KSA, microscopic diagnosis
|How to cite this article:|
Zaki WM, Madkhali AM. Accuracy of immunochromatography diagnostic test versus microscopy in the diagnosis of malaria among clinically suspected patients in Jazan area, KSA. Parasitol United J 2016;9:95-102
|How to cite this URL:|
Zaki WM, Madkhali AM. Accuracy of immunochromatography diagnostic test versus microscopy in the diagnosis of malaria among clinically suspected patients in Jazan area, KSA. Parasitol United J [serial online] 2016 [cited 2018 May 23];9:95-102. Available from: http://www.new.puj.eg.net/text.asp?2016/9/2/95/205164
| Introduction|| |
Malaria is a critical disease leading to high mortality and morbidity in endemic countries . The WHO recorded 214 million malaria cases with about 438 000 deaths in 2015, especially among children . P. falciparum accounts for most deaths from malaria and it is the most indigenous Plasmodium spp. in Saudi Arabia ,. Jazan region is considered an endemic area for malaria where the prevalence is higher in southern than in other regions . Data collected from the malaria health records in KSA indicated the diagnosis of 1236 malaria cases per 100 000 inhabitants in 1992, which decreased to 276 cases in 2000 . In 2003, more than 70% of total national case burden occurred in the southern region, mainly Jazan and Asir, of which about 90% were caused by P. falciparum meanwhile, in Yemen, a country that shares border with Jazan, the predominance of P. falciparum, was noted . The high morbidity and mortality of the disease are due to development of parasite resistance to antimalarial drugs . This was also attributed to mosquito vector resistance to the insecticides used . However, as designated, malaria can be considered curable if accurate, rapid diagnosis was achieved and followed promptly by treatment . As the clinical approach is usually insufficient, available laboratory tests are relied on for the diagnosis . These laboratory tests include microscopic examination of Giemsa-stained thin and thick blood films, which, as recommended by the WHO , is the gold standard for the diagnosis of malaria. However, microscopic examination is met with the obstacle of lack of skilled microscopists in endemic areas, which leads to poor interpretation of data . Microscopy is also time-consuming and laborious, cannot detect sequestered P. falciparum parasites, and is unreliable at low-density parasitemia (50 parasites/ml blood) . Some other techniques such as quantitative buffy coat and PCR have a wide range of accuracy but require expensive equipments and materials that may not always be available for diagnosis in endemic areas. In addition, serologic tests for antibody detection cannot differentiate between old and current infection, especially in malaria-endemic areas . All these restrictions led to the search for consistent simple and cost-effective rapid diagnostic tests (RDT) for the detection of malaria parasites that are as diagnostic as microscopy . As a result, researchers succeeded in introducing a RDT based on the capture of the malaria parasite antigen from peripheral blood using monoclonal antibodies . Because the histidine-rich protein 2 (HRP-2), expressed on the infected red blood cell membrane surface, is very stable  and abundant in P. falciparum, it was the first antigen used for the development of a malaria RDT . Another effectively used antigen is the lactate dehydrogenase (pLDH) soluble enzyme in the glycolytic pathway of the malaria parasites produced by both sexual and asexual stages of all Plasmodium spp. . The pLDH activity was found to correlate with the level of parasitemia in vitro cultures as well as in the plasma of infected patients . Several other enzymes of the malaria parasite glycolytic pathway, notably aldolase, were suggested as target antigens for RDT for species other than P. falciparum .
In the present study, we aim to evaluate the performance characteristics of the BinaxNOW® – ICT malaria test versus blinded microscopic analysis of Giemsa-stained blood films from susceptible malaria patients in Jazan region, KSA, and confirm its validity for use as a RDT.
| Materials and methods|| |
This is an analytic prospective study that follows the guidelines of the Standards for Reporting Diagnostic Accuracy (STARD) for assessment of the validity of diagnostic tests .
Study population and design
The current study included 200 clinically suspected malaria patients attending three general hospitals in Jazan region (Jazan, Abu-Arish, and El-Arda) during the period between April 2014 and March 2015. Selection of patients was based on the complaint of prolonged fever or history of fever in the last 48 h with no other evident cause for fever, no recent history of malaria treatment or past history of malaria. Inclusion in the study depended on the results of Giemsa-stained thin and thick blood films. Microscopy and RDT were performed in parallel for all specimens, and the test results were conveyed to the physicians for final diagnosis.
Thin and thick blood films were prepared directly from finger prick blood samples of the patients recruited in the study and stained with 10% diluted Giemsa stain. The thick blood films were prepared for spot diagnosis of infection, followed by species identification in Giemsa-stained thin blood films . A slide was considered positive when one parasite was found. After that, the other 200 fields were completed for the detection of any mixed infection. If no parasite was found in 200 oil fields, the slide was considered negative. Thick blood smears were used for parasite density measurement by counting the number of parasites per 200 leukocytes and expressed as parasites/µl. When the parasitic count was 10 or less, 500 leukocytes were counted .
ICT of 15 μl finger prick capillary blood was carried out using the BinaxNOW® (Alere Scarborough Inc., Scarborough, Maine, USA) malaria test for the qualitative detection of circulating P. falciparum antigen and a pan-malaria antigen in the whole blood. The test card contains immobilized antibodies specific for the HRP-2 antigen of P. falciparum and antibodies specific for the aldolase pan-malaria antigen. The assay was performed according to the manufacturer’s instructions. The test results were independently examined and interpreted by two observers unaware of the microscopic results. The final results of the test were recorded as either negative or positive. The results were interpreted by the presence or absence of visually detectable pink-to-purple colored lines. A positive test result was based on the detection of both test and control lines. A negative test result produced only a control line, indicating that those malarial antigens were not detected in the sample. Failure of the control line to appear despite the presence of one or both test lines indicated an invalid result that was then excluded from the positive cases.
Diagnosis of P. falciparum malaria was made if the HRP-2 line (T1 line) was visible, with or without the pan-malarial antigen line. A diagnosis of other Plasmodium spp. was made if only the pan-malarial antigen line (T2 line) was visible. Coinfection with both P. falciparum and P. vivax or any other malaria species cannot be distinguished from P. falciparum alone when both T1 and T2 lines are visible. For qualitative detection of circulating P. falciparum antigen and pan-malaria antigen, a scoring system for test line intensities was designed with a standard reference chart . Line intensity was graded into four categories compared with control line: faint (very light), weak (lighter than control line), dense (equal to control line), and very dense (stronger than control line). Each positive line was very closely matched to this chart ([Figure 1]). The clinical limit of detection of P. falciparum was described in the manufacturer’s test kit product instructions to be 1001–1500 parasites/μl, and for other species it was determined as 5001–5500 parasites/μl.
Statistical analysis was performed with the SPSS version 16 (Chicago, Illinois, USA). Specimens were classified as true-positive, true-negative, false-positive, and false-negative result for each sample under evaluation compared with the microscopy reference standard. Specificity, sensitivity, positive and negative predictive values, and diagnostic accuracy were calculated. Comparisons were evaluated using the χ2-test; P value less than 0.05 was considered significant. For analyzing the agreement between the two diagnostic tests, the Cohen’s kappa (κ) test was used. Spearman correlation was also applied between the parasitemia and the reading of the intensity of the ICT diagnostic band. All parameters were estimated with a 95% confidence interval.
All patients included in the study were informed about the aim of the study and an approval form was used to obtain written informed consent from each participant or their parents. Positive malaria patients were informed of their results and appropriate treatment was prescribed by the physician concerned.
| Results|| |
A total of 200 samples from 97 male (48.5%) and 103 female patients (51.5%) were analyzed. Their ages ranged from 3 to 74 years, with a mean age of 19.8±2.1 years. Microscopic examination of thin and thick Giemsa-stained blood films revealed that 64 cases (32%) were positive for Plasmodium spp. The positive cases comprised 35 male (17.5%) and 29 female patients (14.5%); their ages ranging from 3 to 71 years, with a mean age of 19.4±1.8 years. The majority (73%) of the affected age group comprised adults, 19–43 years of age. Meanwhile, 43/64 cases (67.19%) were positive for single infection with P. falciparum ([Figure 2]), and 12/64 (18.75%) had mixed infection with P. falciparum. Other Plasmodium spp. were detected in the remaining nine cases (14.06%), of which eight cases were of P. vivax (12.5%) and one case was of P. ovale (1.56%). In single and mixed P. falciparum infections, asexual stages with or without sexual forms were observed in 51/64 samples (79.6%) ([Figure 2]a) and only P. falciparum sexual gametocyte stages were present in 4/64 samples (6.3%) ([Figure 2]b).
|Figure 2 Blood smear showing (a) P. falciparum ring stage in a thick blood film and (b) P. falciparum gametocyte in a thin blood film.|
Click here to view
With the BinaxNOW® malaria test, the control bands appeared for all tested samples, whether with positive or negative results, except for one case in which only the T1 test line appeared; thus, it was considered as an invalid result according to the manufacturer’s instructions ([Figure 3]c). The ICT diagnosed 66/200 (33%) cases positive for any of the Plasmodium spp. (34 male and 32 female; 51.5 and 48.5%, respectively). Their ages ranged from 3 to 69 years, with a mean age of 18.6±1.9 years. From the 66 positive cases, 36 (54.5%) were diagnosed as single infection with P. falciparum, indicated by positive T1 line (HRP-2 antigen) ([Figure 3]a), 21 (31.8%) as mixed infection with P. falciparum, indicated by positive T1+T2 lines (HRP-2 antigen plus aldolase antigen) ([Figure 3]b), and nine (13.6%) as infection with other Plasmodium spp., indicated by positive T2 line (aldolase antigen).
|Figure 3 Results of ICT HRP-2: a: Positive P. falciparum, b: Positive mixed infection, c: Invalid.|
Click here to view
The intensity of the 66 positive lines was considered as faint, weak, dense, and very dense in 14 (20.9%), 31 (45.5%), 19 (28.4%), and 3 (4.5%) cases, respectively ([Figure 1] and [Table 1]).
|Table 1 Distribution of malaria patients and level of parasitemia according to the intensity of Binax Now® ICT line color|
Click here to view
The ICT showed five false-positive samples for P. falciparum infection and two false-negative samples, one of which was diagnosed microscopically as P. falciparum infection and the other as P. vivax infection ([Table 2]). The intensity of ICT bands directly correlated with the level of parasitemia observed by means of microscopy (Spearman ρ=0.76), indicating a positive relationship between band intensity and level of parasitemia.
|Table 2 Comparison of Binax Now® ICT and microscopic examination results (n=200)|
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The overall sensitivity and specificity of the ICT in detecting any Plasmodium spp. compared with microscopy were 97% (with 89–99.6%: 95% confidence interval) and 96% (with 91.6–98.8%: 95% confidence interval), respectively ([Table 3]).
|Table 3 Performance characteristics of BinaxNow® ICT in patients with a presumptive malaria clinical diagnosis|
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To analyze the reliability of the ICT for the detection of single P. falciparum infection, the mixed infections diagnosed by means of microscopy were not taken into account, whereas in the ICT both single P. falciparum (HRP-2 specific antigen) and mixed infections were included in the analysis. As regards P. falciparum single infection, the sensitivity and specificity of the ICT were 96.7% and 78%, respectively, the positive and negative predictive values were 92.5% and 98%, respectively, and the diagnostic accuracy was 95.8%. The sensitivity of the ICT in detecting Plasmodium spp. other than P. falciparum compared with microscopy was 91.6% and the specificity was 100%. Meanwhile, positive and negative predictive values increased with an increase in parasitemia ([Table 3]), and the diagnostic accuracy was 99%.
| Discussion|| |
Most malaria-endemic areas depend on clinical grounds for diagnosis, which although sensitive, is unreliable, not specific, and may lead to misdiagnosis . Consequently, laboratory-confirmed diagnosis was strongly recommended by the WHO . In recent years, RDTs have emerged as a promising alternative to microscopy . It was recommended that a RDT must have the following characteristics: high sensitivity to ensure detection of all clinically significant malaria infections; high specificity to enable monitoring low malaria prevalence and appropriate management of nonmalarial fever; and high stability to allow transport and storage in ambient conditions in malaria-endemic areas .
In the present study, the percentage of positive cases by means of microscopic examination was 32% (17.5% male and 14.5% female) and that using the ICT was 33% (51.5% male and 48.5% female). Although insignificant, the observed relatively higher male-to-female ratio was also recorded in Ethiopia where male population was more frequently affected compared with female population, with infection rates of 52.6 and 47.3%, respectively . Nearly 73% of our malaria patients were adults (19–43 years) which is similar to that reported in Ethiopia by Mengistu and Diro , who observed that 75% of infected patients were in this age group. Moreover, in India, it was found that 66.7% of patients lie in the same age group due to higher exposure to mosquito bites as compared with older generations who appear to acquire partial immunity to malaria with increasing age, especially in endemic areas . A previous study conducted in Indonesia, which compared the sensitivity of an HRP-2 assay in children and adults, demonstrated its higher sensitivity in children. This was attributed to lower immunity and possible lesser antibody interference . Another study rightfully recommended parasitological confirmation in suspected children under 5 years of age . It was proposed that specific identification of malaria parasites species is of vital importance, permitting early therapeutic intervention particularly with relapsing P. vivax and P. ovale malaria, and in P. falciparum infection because it is usually accompanied by severe morbidity and mortality .
In our study, species identification by means of microscopy showed that the majority of malaria cases were caused by P. falciparum (85.9%) either in a pure form (67.19%) or as a mixed infection (18.75%), and the remaining (14.06%) cases were caused by either pure P. vivax (12.5%) or P. ovale (1.56%). This is in accordance with other studies that revealed that infection with P. falciparum is the most prevalent type among malaria-infected Saudi patients, especially in Jazan, which is considered as an endemic area for this species ,, followed by P. vivax . However, a study conducted in El-Taif, KSA, revealed that P. vivax is the most prevalent species, followed by P. falciparum . The P. ovale case which was reported in the current study may be imported malaria. The variability in malaria species prevalence among different areas depends on geographical, environmental, and seasonal factors.
In the current study, the BinaxNow® test was apparently false-positive in five P. falciparum samples that were negative with microscopy. A previous comprehensive study explained that these false positives are due to persistence of circulating HRP-2 antigen for up to 28 days after antimalarial treatment , resulting in false-positive results. Other causes may be persistence of antigens due to sequestration of malaria parasites from peripheral blood , incomplete treatment, delayed clearance of circulating antigen (free or in antigen–antibody complexes), and cross-reaction with non-P. falciparum malaria, serum rheumatoid factor , or heterophile antigen . Moreover, false-positive results may be produced in highly malaria-endemic areas when parasitemia level is low with absent clinical manifestations . However, in our study, this assumption is unlikely to occur because all those included in the study had fever.
The present study showed false-negative results of RDTs for two patients who were microscopically positive, one for P. falciparum and the other for P. vivax. False-negative P. falciparum results have been attributed to possible genetic heterogeneity of HRP-2 expression , deletion or mutation of hrp2 gene, presence of blocking antibodies, or immune-complex formation . Another cause for false-negative BinaxNow® result is low-level parasitemia. However, cases with very high parasitemia may also produce a false-negative BinaxNow® result as a consequence of antigen excess (prozone effect). Previous studies have demonstrated a prozone effect with parasitemia loads greater than 4% as a result of excess HRP-2 antigen, which interferes with binding of the antibody, leading to false-negative results . Other studies assessing BinaxNow® sensitivity and specificity showed a range of accuracy (from 86 to 100% and from 84 to 99%, respectively) ,,,,. The variation may be due to test kit storage conditions in the field, inadequate adherence to the test protocol, or levels of parasitemia below the detection limit of the test. In addition, the use of different gold-standards and possible geographic variation in malaria antigens may contribute to these variations. Farcas et al.  conducted a study for the evaluation of the BinaxNow® ICT in malaria detection and showed that it gave a low sensitivity of 61.5% for the detection of pure P. malariae and P. ovale infections, which was attributed to either low parasite count in these infections or a low expression of the ‘pan-malarial’ antigen by both these malaria species. However, in another study, the sensitivity of BinaxNow® ICT for detecting P. falciparum in mixed infection or in its pure form was 96 and 98%, respectively . In our study, the sensitivity and specificity of BinaxNow® ICT for detecting non-P. falciparum malaria was 91.6% and 78%, respectively, taking into consideration that P. falciparum infection accounts for almost 99% of malaria infections in the study area ,; therefore, the low sensitivity of the BinaxNow® ICT for non-P. falciparum malaria may not be a serious cause for concern in Jazan area.
In the present study, the overall sensitivity and specificity of the test was 97% and 96%, respectively, but when it was measured for P. falciparum in its pure or mixed form it was 96.7 and 78%, respectively, and, when mixed P. falciparum infection is excluded, the specificity will be 97%. The decreased specificity, when mixed infection was included, was attributed to the inability of the test to discriminate between P. falciparum single and mixed infections ,.
In non-P. falciparum malaria, the sensitivity of the test was 100% at a high level of parasitemia (>10 000 parasites/µl), but dropped to 66.6% when the level was below 1000 parasites/µl.
Line intensity grading was positively correlated with the level of parasitemia, as shown by Spearman P=0.76 positive value for the intensity of grading in relation to the level of parasitemia. This finding is in accordance with other studies, which stated that line intensities were related to parasite density ,,. Tjitra et al.  stated that line intensities for the HRP-2 antigen and particularly the panmalarial antigen were associated with parasite density. Another opinion stated that the semiquantitative estimation of plasma parasite antigens may be useful for the rapid prediction of parasite biomass .
According to the manufacturer’s instructions, appearance of the control line is essential for validation of the test, but we had one case in which there was a positive T1 line (HRP-2 line) without the presence of control line ([Figure 3]c). Although it was repeated twice with the same lot of kits, the same interpretation was noted, and it was confirmed positive by means of microscopic examination. Moreover, the same result was obtained in a study by Durand et al. , who hypothesized that an inhibitor may be present in the blood, preventing high-quality development of the assay, which may have happened in the present study.
Authors’ contribution: WM Zaki proposed the research idea and design of the work; she made contributions to laboratory procedures and acquisition of data, and prepared the final version for submission. AM Madkhali shared in designing the study, sample collection, and revision of thewritten article. Both authors revised and approved the final version submitted for publication.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]