Use of the Rapid BinaxNOW Malaria Test in a 24-Hour Laboratory Associated with
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1 JCM Accepts, published online ahead of print on 13 February 2013 J. Clin. Microbiol. doi: /jcm Copyright 2013, American Society for Microbiology. All Rights Reserved Use of the Rapid BinaxNOW Malaria Test in a 24-Hour Laboratory Associated with Accurate Detection and Decreased Malaria Testing Turnaround Times in a Non-Endemic, Pediatric Setting K. V. Ota 1,2,# D. Blecker-Shelly 1 1 The Children s Hospital of Philadelphia, Philadelphia, USA 2 Perelman School of Medicine, University of Pennsylvania, Philadelphia, USA Running title: Rapid Malaria Testing in Pediatrics Keywords: Pediatric, Malaria, Rapid Testing, Diagnosis #Corresponding Author: Dr. Kaede Ota, M.D., M.Sc. The Children s Hospital of Philadelphia 34 th Street and Civic Center Boulevard Main Building, Room 5112A Philadelphia, Pennsylvania, USA Tel: Fax: otak@ .chop.edu
2 Abstract The impact of implementing the BinaxNow malaria test (RDT) was evaluated. From 288 tests, 34 malaria cases were detected. Laboratory turnaround time decreased from 9.8 to 1.7 hours for report of any Plasmodium spp, 10.2 to 1.6 hours for P. falciparum and 8.6 to 1.1 hours for any result. 2
3 Therapeutic delay has been associated with increased risk of mortality in Plasmodium falciparum malaria 1 Timely administration of anti-malarial therapy is in turn, dependent on swift clinical identification of persons at risk, prompt specimen acquisition and rapid testing turnaround time. The BinaxNOW Malaria test (RDT; Alere Scarborough, Inc., Scarborough, ME) is a Food and Drug Administration-approved immunochromatographic assay that detects P. falciparum-specific histidine-rich protein 2, and aldolase, a pan-plasmodium enzyme within 20 minutes. We investigated its performance in a pediatric population in a non-endemic setting and its impact on malaria testing turnaround times. All specimens received for malaria testing from January 1, 2006 to December 31, 2011 inclusive were considered for inclusion. Only the first specimen submitted, per patient, was analyzed. We recorded the date and time of specimen receipt and first report of any result (the presence of Plasmodium falciparum or a non-falciparum species or the absence of Plasmodium spp.); RDT and thick and thin Giemsa smear results; shift (day shift versus evening or night shift) and staffing status (standard week day versus holiday or weekend) at the time of specimen receipt. Medical records of all cases were reviewed to determine if they met the Centers for Disease Control and Prevention s criteria for severe malaria (one or more of the following criteria: impaired consciousness/coma, severe normocytic anemia (hemoglobin < 7 g/dl), renal failure, acute respiratory distress syndrome, hypotension, disseminated intravascular coagulation, spontaneous bleeding, acidosis, hemoglobinuria, jaundice, repeated generalized convulsions, and/or parasitemia of 5%).. 2 3
4 A protocol involving RDT followed by thick and thin Giemsa smear microscopy was implemented on August 1, Prior to this, we relied solely on thick and thin smears for malaria diagnosis. Testing was performed on venous blood anti-coagulated in EDTA. RDT was performed according to manufacturer s instructions. Two thin and two thick Giemsa smears were prepared from every blood specimen and positive smears were reviewed by two technologists. Throughout, the policy was for thick and thin smears to be prepared and read as soon as a technologist with the necessary skills started his/her shift. RDT was performed immediately upon specimen receipt, results were reported as preliminary and finalized when blood smear results were reported. All technologists performed RDT but only microbiology technologists prepared and read blood smears. 288 specimens (67 pre-rdt, 221 post-rdt) qualified for analysis. There were 34 confirmed cases of malaria with positive RDT and blood smears. Blood smears were positive in nine of the 67 patients tested pre-rdt (seven P. falciparum; one P. vivax; one P. ovale). After introduction of RDT, 27 of the 221 patients tested were RDT-positive. Blood smears yielded 19 cases of P. falciparum malaria; three P. vivax; two P. ovale; and one mixed case with P. falciparum and P. ovale. Of the 27 P. falciparum cases with parasites seen on blood smears, 16 had <1% parasitemia. The remaining 11 cases had 1.2, 2.2, 6.1, 6.3, 6.5, 6.9, 10.1, 15.0, 17.0, 20.4 and 35% parasitemia. In two cases, RDT tested positive for P. falciparum but no parasites were seen on blood smears. Both cases presented febrile and defervesced with atovaquoneproguanil therapy. Neither had an alternative diagnosis to explain the fever. One case arrived in the United States from a refugee camp in Thailand three months prior to presentation. Two subsequent sets of thick and thin smears showed no evidence of Plasmodium species. The second case had a travel history to Nigeria three weeks prior to presentation during which she reportedly 4
5 took malaria prophylaxis. Compliance was not documented. A subsequent blood smear was negative for Plasmodium spp. Both cases were analyzed as false positives. Nine cases with P. falciparum malaria met CDC criteria for severe malaria and all had parasitemia levels >5%. Five cases met other criteria for severe malaria (hypotension, hemoglobin levels < 7g/dL). Using Giemsa smears as the gold standard, the SN, SP, PPV and NPV of RDT were 100%, 99%, 92% and 100% respectively for the detection of any Plasmodium spp. and 100%, 99%, 91% and 100% for P. falciparum. RDT detected 5/5 cases of P. vivax and P. ovale. The mixed infection with P. falciparum and P. ovale was analyzed as P. falciparum malaria. Univariate and multivariate analysis results comparing TAT pre-rdt and post-rdt are summarized in Table 1. Mean TAT to an actionable malaria report (P. falciparum or nonfalciparum malaria) was shorter post-rdt than pre-rdt (1.7 hours versus 9.8 hours; p<0.001) as was mean TAT to a report of P. falciparum malaria (1.6 hours versus 10.2 hours; p<0.001) and mean TAT to any result, positive or negative (1.1 hours versus 8.6 hours; p<0.001). Using multivariate linear regression modeling, overall TAT in specimens received in the post-rdt era remained significantly shorter compared to specimens received pre-rdt after adjusting for shift and staffing (p<0.001). We detected 34 cases of malaria over 6 years in a non-endemic, tertiary, pediatric center. 9 cases met CDC criteria for severe malaria. These findings affirmed the value of allocating resources to support continuous, 24/7 malaria testing at our institution. The propensity of RDT toward false at parasite loads <1 000 parasites/μl (or 0.2% parasitemia) is documented in the literature. 3 This limitation is important as non-immune individuals can be symptomatic at parasitemia levels in this range. Children living the United 5
6 States who travel to malaria endemic areas without prophylaxis fall in this group. In our cohort, RDT detected all 34 cases of malaria with a sensitivity of 100%, which is consistent with RDT performance data in the literature. 3-7 Because we did not retain records of exact parasitemia levels below 1%, we were unable to assess the lower limit of detection of RDT in our population. We therefore counsel clinicians to ensure that additional specimens be collected following a negative result when malaria is strongly suspected. There were two cases in which HRP-2 was positive on RDT, but blood smears were negative for parasites. Both cases had a travel history to a malaria-endemic area and responded clinically to anti-malarial therapy. Molecular diagnostics were not pursued to adjudicate the findings as false-positive RDT results or false-negative blood smears. These cases highlighted the utility of molecular diagnostics, when available, to resolve discordance between RDT and microscopy. We did not observe any cases of P. falciparum malaria misidentified by RDT as non-falciparum malaria as reported by DiMaio et al. 8 Introduction of RDT decreased mean TAT from 9.8 to 1.7 hours for any positive malaria result; 10.2 to 1.6 hours for a positive P. falciparum result; and 8.6 to 1.1 hours for all results. The TATs were unusually long pre-rdt. We believe that this was related to inconsistent availability of microbiology technologists skilled at preparing Giemsa stain, preparing slides and reading blood smears. The result was delayed specimen processing. Because all technologists were able to perform RDT, implementation vastly expedited preliminary reporting of all results. Our study had some limitations. First, because of the small sample size (n=34 cases), our multivariate analysis was restricted to evaluation of TAT to any result (positive or negative) as opposed to TAT to positive results, the more clinically relevant outcome. Second, technologists 6
7 reading blood smears were not blinded to RDT results, which may have artificially elevated concordance between RDT and microscopy. While microscopy remains essential for determination of parasite loads, detection of lowlevel parasitemia and mixed infections, we conclude that RDT may be useful in non-endemic settings that evaluate pediatric patients at risk of P. falciparum malaria. RDT appeared highly sensitive and specific for the detection of P. falciparum malaria in our pediatric population and provided a user-friendly platform that allows reporting of actionable malaria testing results in a STAT manner as recommended by national guidelines. 9 7
8 References 1. Newman, R.D., M. E. Parise, A. M. Barber, R. W. Steketee Malaria-related deaths among U.S. travelers, Ann Intern Med. 141: Centers for Disease Control and Prevention Treatment of Malaria (Guidelines for Clinicians, United States). clinicians2.html. Accessed 5 February Farcas, G. A., K. J. Zhong, F. E. Lovegrove, C. M. Graham, K. C. Kain Performance endemic Evaluation of the Binax NOW ICT test versus polymerase chain reaction and microscopy for the detection of malaria in returned travelers. Am J Trop Med Hyg. 69: Nkrumah, B., S. E. K. Acquah, L. Ibrahim, J. May, N. Brattig, E. Tannich, S. Blay Nguah, Y. Adu-Sarkodie, F. Huenger Comparative evaluation of two raid field tests for malaria diagnosis: Partec Rapid Malaria Test and Binax Now Malaria Rapid Diagnostic Test. BMC Infect Dis. 11: Stauffer, W. M., C. P. Cartwright, D. A. Olson, B. A. Juni, C. M. Taylor, W. H. Bowers, K. L. Hanson, J. E. Rosenblatt, D. R. Boulware Diagnostic Performance of Rapid Diagnostic Tests versus Blood Smears for Malaria in US Clinical Practice. Clin Infect Dis. 49:
9 Wiese, L., B. Bruun, L. Baek, A. Friis-Møller, B. Gahrn-Hansen, J. Hansen, O. Heltberg, T. Højbjerg, M. K. Hornstrup, B. Kvinesdal, G. Gomme, J. A. Kurtzhals Bedside diagnosis of imported malaria using the Binax Now malaria antigen detection test. Scand J Infect Dis. 38: De Monbrison, F., P. Gérome, J. F. Chaulet, M. Wallon, S. Picot, F. Peyron Comparative diagnostic performance of two commercial rapid tests for malaria in a nonendemic area. Eur J Clin Microbiol Infect Dis. 23: DiMaio, M.A., I. T. Pereira, T. I. George, N. Binaei Performance of BinaxNOW for Diagnosis of Malaria in a U.S. Hospital. J Clin Microbiol. 50: CLSI Laboratory Diagnosis of Blood-borne Parasitic Diseases; Approved Guideline. CLSI document M15A. Wayne, PA: Clinical and Laboratory Standards Institute. Acknowledgments: We thank Ms. Lan Nguyen for her technical input, Dr. Karin McGowan for her input into the multivariate analyses, and Ms. Michelle Precourt for her assistance with data acquisition. Conflicts of interest: None to declare. Author Contributions: K.V.O. contributed to the conception and design of this study; data collection; data analysis; and drafted and edited the manuscript. D.B.S contributed to the conception and design of this study; data analysis; and edited the manuscript. 9
10 Table 1. Univariate and multivariate analysis results of the characteristics of malaria testing preand post-implementation of the Binax NOW malaria test (RDT) Pre-RDT (n=67) Post-RDT (n=221) p-value (unadjusted) p-value (adjusted) Mean TAT to a positive report 1 (SE) Mean TAT to a P. falciparum report 1 (SE) Mean TAT to any report 2 (SE) 9.8 hours (2.4) 10.2 hours (2.8) 8.6 hours (0.84) 1.7 hours (0.43) 1.6 hours (0.52) 1.1 hours (0.14) < n/a < n/a < <0.001 % tests received on day shift 3 50% 58% % tests received when fully staffed 4 77% 76% Turnaround time to a positive report: the time elapsed from specimen receipt in the Microbiology Laboratory to the first report of P. falciparum or non-falciparum malaria. 2. Turnaround time to any report: the time elapsed between specimen receipt in the Microbiology Laboratory to the report of any result, positive or negative. 3. Day shift was defined as 08:00 to 15:59; evening shift 16:00 to 23:59; night shift midnight to 06: Fully staffed was defined as any work day that was not Saturday or Sunday (ie. a weekend) or a hospital-designated holiday. 5. By Student s T-test. 6. By Chi-square test for proportions. 1
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