Detection of SARS-CoV-2 through pool testing for COVID-19: an integrative review

Costa, Murilo Soares; Guimarães, Nathalia Sernizon; Andrade, André Barbosa de; Vaz-Tostes, Luiza Passini; Oliveira, Rhuan Braga; Simões, Madara da Silva; Gelape, Gabriel de Oliveira; Alves, Claudia Regina Lindgren; Machado, Elaine Leandro; Fonseca, Flávio Guimarães da; Teixeira, Santuza Maria Ribeiro; Sato, Hugo Itaru; Takahashi, Ricardo Hiroshi Caldeira; Tupinambás, Unaí

doi:10.1590/0037-8682-0276-2021

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Review Article • Rev. Soc. Bras. Med. Trop. 54 • 2021 • https://doi.org/10.1590/0037-8682-0276-2021 copy

Detection of SARS-CoV-2 through pool testing for COVID-19: an integrative review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

INTRODUCTION:

The pool testing technique optimizes the number of tests performed and reduces the delivery time of results, which is an interesting strategy for the health crisis caused by the COVID-19 pandemic. This integrative review investigated studies in which pool testing was carried out for epidemiological or screening purposes to analyze its clinical or cost effectiveness and assessed the applicability of this method in high-, middle-, and low-income countries.

METHODS:

This integrative review used primary studies published in the MEDLINE, EMBASE, Literatura Latino-Americana e do Caribe em Ciências da Saúde (LILACS), and Cochrane Library databases.

RESULTS:

A total of 435 studies were identified: 35.3% were carried out in Asia, 29.4% in Europe, 29.4% in North America, and 5.9% in Oceania.

CONCLUSIONS:

This review suggests that pool testing in the general population may be a useful surveillance strategy to detect new variants of SARS-CoV-2 and to evaluate the period of immunogenicity and global immunity from vaccines.

Keywords:
COVID-19; SARS-CoV-2; Pool testing; Diagnosis; Pandemic

Reference	Institute	Journal	Country	Population	Study category	Type of information
Abdalhamid et al. ¹⁸18. Abdalhamid B, Bilder CR, McCutchen EL, Hinrichs SH, Koepsell SA, Iwen PC, et al. Assessment of specimen pooling to conserve SARS CoV-2 testing resources. Am J Clin Pathol. 2020;153(6):715-8.	University of Nebraska	AJCP	USA	People at risk for COVID-19	Special article	Cross-sectional: Screening
Ben-Ami et al. ¹⁹19. Ben-Ami R, Klochendler A, Seidel M, Sido T, Gurel-Gurevich O, Yassour M, et al. Large-scale implementation of pooled RNA extraction and RT-PCR for SARS-CoV-2 detection. Clin Microbiol Infect. 2020;26(9):1248-53.	The Hebrew University of Jerusalem	Clinical Microbiology and Infection	Israel	Asymptomatic	Original article	Cross-sectional: Screening
Chong et al. ²⁰20. Chong BSW, Tran T, Druce J, Ballard SA, Simpson JA, Catton M. Sample pooling is a viable strategy for SARS-CoV-2 detection in low-prevalence settings. Pathology. 2020;52(7):796-800.	Victorian Infectious Diseases Reference Laboratory; University of Melbourne	Pathology	Australia	Hospital inpatients, healthcare workers	Brief report	Cross-sectional: Screening
Garg et al. ²¹21. Garg J, Singh V, Pandey P, Verma A, Sen M, Das A, et al. Evaluation of sample pooling for diagnosis of COVID‐19 by real time‐PCR: A resource‐saving combat strategy. J Med Virol . 2020;93(3):1526-31.	Dr. Ram Manohar Lohia	Journal of Medical Virology	India	General sample in areas with varying prevalence of population referred to COVID laboratory	Original article	Cross-sectional: Screening
	Institute of Medical Science
Hogan et al. ²²22. Hogan CA, Sahoo MK, Pinsky BA. Sample pooling as a strategy to detect community transmission of SARS-CoV-2. JAMA Netw Open . 2020;323(19):1967-69.	Stanford University	JAMA Network Open	USA	Patients with flu-like symptoms	Letter	Cross-sectional: Screening
	School of Medicine
Jung et al. ²³23. Jung J, Kim M-N, Kim S-H. Universal screening with sample pooling in preoperative patients as long-term strategy in the COVID-19 pandemic. J Korean Med Sci. 2020;35(33):e309.	University of Ulsan	JKMS	South Korea	Preoperative patients	Opinion	Cross-sectional: Screening
	College of Medicine
Lim et al. ²⁴24. Lim KL, Johari NA, Wong ST, Khaw LT, Tan BK, Chan KK, et al. A novel strategy for community screening of SARS-CoV-2 (COVID-19): Sample pooling method. PLoS One. 2020;15(8):e0238417.	International Medical University	PLoS ONE	Malaysia	Contact tracing for COVID-19	Original article	Cross-sectional: Inquiry
Lohse et al. ²⁵25. Lohse S, Pfuhl T, Berkó-Göttel B, Gärtner B, Becker SL, Schneitler S, et al. Challenges and issues of SARS-CoV-2 pool testing - Authors’ reply . Lancet Infect Dis . 2020;20(11):1234-5.	Saarland University Medical Center	The Lancet Infectious Diseases	Italy	Asymptomatic	Letter	Cross-sectional: Screening
Mastrianni et al. ²⁶26. Mastrianni D, Falivena R, Brooks T, McDermott B, Tan J, Vandell R, et al. Pooled Testing for SARS-CoV-2 in hospitalized patients. J Hosp Med. 2020;15(9):538-9.	Saratoga Hospital	Journal of Hospital Medicine	USA	Patients at low risk of SARS-CoV-2 infection	Brief report	Cross-sectional: Screening
Möckel et al. ²⁷27. Möckel M, Thibeault C, Stein A, Hofmann J, Gastmeier P. Daily pool testing of nasopharyngeal self-obtained swaps of healthcare professionals with definite COVID-19 exposition. Eur J Emerg Med. 2020;27(4):301-2.	Universitätsmedizin Berlin	European Journal of Emergency Medicine	Germany	Health professionals	Letter	Case report
Mohanty et al. ²⁸28. Mohanty S, Ravindra A, Gupta K, Hallur V, Behera B, Mahaptra A, et al. Intricacies in characterizing positivity in pooled sample testing for SARS-CoV-2. J Med Virol . 2021;93:2799-804.	India Institute of Medical Sciences	Journal of Medical Virology	India	Asymptomatic or symptomatic people that had contact with infected patients	Original article	Cross-sectional: Screening
Petrucca et al. ²⁹29. Petrucca A, Borro M, Lionetto L, Gentile G, Alari A, Simmaco M, et al. Validation of a small-size pooling approach targeting hospital surveillance of SARS-CoV-2 infection. Infect Control Hosp Epidemiol. 2020;1-2.	Sant’Andrea Hospital; University of Rome	Infection Control and Hospital Epidemiology	Italy	Health professionals	Letter	Cross-sectional: Screening
Schmidt et al. (30)	German Red Cross Blood Transfusion Service; Goethe-University	Transfusion	Germany	Symptomatic patients and asymptomatic employees	Original article	Cross-sectional: Screening
Denny et al. ³¹31. Denny TN, Andrews L, Bonsignori M, Cavanaugh K, Datto MB, Deckard A, et al. Implementation of a pooled surveillance testing program for asymptomatic SARS-CoV-2 infections on a college campus - Duke University, Durham, North Carolina, August 2-October 11, 2020. MMWR Morb Mortal Wkly Rep, 2020;69(46):1743-7.	Duke University	Morbidity and Mortality Weekly Report	USA	Asymptomatic	Brief Report	Cross-sectional: Screening
Kim et al. ¹¹11. Kim SY, Lee J, Sung H, Lee H, Han MG, Yoo CK, et al. Pooling upper respiratory specimens for rapid mass screening of COVID-19 by real-time RT-PCR. Emerg Infect Dis. 2020;26(10):2469-72.	Asan Medical Center; University of Ulsan College of Medicine	JKMS	South Korea	Health professionals	Brief Report	Cross-sectional: Screening
Schneitler et al. ³²32. Schneitler S, Jung P, Bub F, Alhussein F, Benthien S, Berger FK, et al. Simple questionnaires to improve pooling strategies for SARS-CoV-2 laboratory testing. Ann Glob Health, 2020;86(1):148.	Saarland University; University of Cologne	Annals of Global Health	Germany	Police staff, hospital inpatients, and nursing home residents	Original article	Case-control
Wang et al. ³³33. Wang W, Xu Y, Gao R, Lu R, Han K, Wu G, et al. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA. 2020;323(18):1843-4.	Stanford University	Emerging Infectious Diseases	USA	Symptomatic and asymptomatic inpatients and outpatients	Original article	Case-control

Reference	Country	Pools number	Total samples	Number of samples per pool	% Positive pools	% Positive sample	Sensitivity	Specificity
Abdalhamid et al. (2020)	USA	12	60	5	NS	3.33%	95% or 100%	100%
Ben-Ami et al. (2020)	Israel	3.322	26,576	8	NS	0.12%	NS	NS
Chong et al. (2020)	Australia	7.175	29,700	4; 8	0.84%	0.23%	99%	99%
Garg et al. (2020)	India	3.452	19,560	5; 10	7.39%	1.42%	95% or 100%	100%
Hogan et al. (2020)	USA	292	2,888	9; 10	0.68%	0.07%	NS	NS
Jung et al. (2020)	South Korea	NS	37,127	NS	NS	0.30%	NS	NS
Lim et al. (2020)	Malaysia	NS	2,732	5; 7; 10	NS	1.90%	NS	NS
Lohse et al. (2020)	Italy	267	1,191	4; 30	4.24%	1.93%	NS	NS
Mastrianni et al. (2020)	USA	179	530	2-3	2.23%	0.8%	60% to 80%	95% to 99%
Möckel et al. (2020)	Germany	1	10	10	0%	0%	NS	NS
Mohranty et al. (2020)	India	1.807	7,228	4	8.3%	3.47%	NS	NS
Petrucca et al. (2020)	Italy	407	2,035	5	8.84%	1.76%	100%	100%
Schmidt et al. (2020)	Germany	3.210	NS	10; 20; 30; 40; 50	NS	NS	NS	NS
Denny et al. (2020)	USA	NS	59,476	NS	n=158	n=29	NS	NS
Kim et al. (2020)	South Korea	NS	609	5	0%	0%	NS	NS
Schneitler et at. (2020)	Germany	6.012	25,978	5; 10; 13	14.6% (random); 1.2% (questionnaire)	3.5% (random); 0.1% (questionnaire)	NS	NS
Wang et al. (2021)	USA	302	1,648	8; 4	NS	5.83%	95%	NS

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[1] Corresponding author: Dr. Unaí Tupinambás. e-mail:unaitupi@gmail.com