COVID-19 testing

CDC 2019-nCoV Laboratory Test Kit.jpg
The US CDC's COVID-19 laboratory test kit

COVID-19 testing involves analyzing samples to assess the current or past presence of SARS-CoV-2. The two main branches detect either the presence of the virus or of antibodies produced in response to infection.[1][2] Tests for viral presence are used to diagnose individual cases and to allow public health authorities to trace and contain outbreaks. Antibody tests instead show whether someone once had the disease. They are less useful for diagnosing current infections because antibodies may not develop for weeks after infection.[3] It is used to assess disease prevalence, which aids the estimation of the infection fatality rate.[4]

Individual jurisdictions have adopted varied testing protocols, including whom to test, how often to test, analysis protocols, sample collection and the uses of test results.[5][6][7] This variation has likely significantly impacted reported statistics, including case and test numbers, case fatality rates and case demographics.[8][9][10]

Test analysis is often performed in automated, high-throughput, medical laboratories by medical laboratory scientists. Alternatively, point-of-care testing can be done in physician's offices, workplaces, institutional settings or transit hubs.

Methods[]

Explanation of the underlying pathophysiology pertaining to diagnosis of COVID-19[11]

Positive viral tests indicate a current infection, while positive antibody tests indicate a prior infection.[12] Other techniques include a CT scan, checking for elevated body temperature or checking for low blood oxygen level.

Detection of the virus[]

Reverse transcription polymerase chain reaction[]

Polymerase chain reaction (PCR) is a process that amplifies (replicates) a small, well-defined segment of DNA many hundreds of thousands of times, creating enough of it for analysis. Test samples are treated with certain chemicals[13][14] that allow DNA to be extracted. Reverse transcription converts RNA into DNA.

Reverse transcription polymerase chain reaction (RT-PCR) first uses reverse transcription to obtain DNA, followed by PCR to amplify that DNA, creating enough to be analyzed.[14] RT-PCR can thereby detect SARS-CoV-2, which contains only RNA. The RT-PCR process generally requires a few hours.[15]

Real-time PCR (qPCR)[16] provides advantages including automation, higher-throughput and more reliable instrumentation. It has become the preferred method.[17][18]

The combined technique has been described as real-time RT-PCR[19] or quantitative RT-PCR[20] and is sometimes abbreviated qRT-PCR[21] rRT-PCR[22] or RT-qPCR,[23] although sometimes RT-PCR or PCR are used. The Minimum Information for Publication of Quantitative Real-Time PCR Experiments (MIQE) guidelines propose the term RT-qPCR,[24] but not all authors adhere to this.

Samples can obtained by various methods, including a nasopharyngeal swab, sputum (coughed up material),[25] throat swabs,[26] deep airway material collected via suction catheter[26] or saliva.[27][28] Drosten et al. remarked that for 2003 SARS, "from a diagnostic point of view, it is important to note that nasal and throat swabs seem less suitable for diagnosis, since these materials contain considerably less viral RNA than sputum, and the virus may escape detection if only these materials are tested."[29]

The likelihood of detecting the virus depends on collection method and how much time has passed since infection. According to Drosten tests performed with throat swabs are reliable only in the first week. Thereafter the virus may abandon the throat and multiply in the lungs. In the second week, sputum or deep airways collection is preferred.[26]

Collecting saliva may be as effective as nasal and throat swabs,[27] although this is not certain.[30][28] Sampling saliva may reduce the risk for health care professionals by eliminating close physical interaction.[31] It is also more comfortable for the patient.[32] Quarantined people can collect their own samples.[31] A saliva test's diagnostic value depends on sample site (deep throat, oral cavity, or salivary glands).[28] One study found that saliva yielded greater sensitivity and consistency when compared with swab samples.[33]

Viral burden measured in upper respiratory specimens declines after symptom onset.[34]

Isothermal amplification assays[]

Isothermal nucleic acid amplification tests also amplify the virus's genome. They are faster than PCR because they don't involve repeated heating and cooling cycles. These tests typically detect DNA using fluorescent tags, which are read out with specialized machines. CRISPR gene ing technology was modified to perform the detection: if the CRISPR enzyme attaches to the sequence, it colors a paper strip. The researchers expect the resulting test to be cheap and easy to use in point-of-care settings.[35][36] The test amplifies RNA directly, without the RNA-to-DNA conversion step of RT-PCR.[37]

Antigen[]

An antigen is the part of a pathogen that elicits an immune response. Antigen tests look for antigen proteins from the viral surface. In the case of a coronavirus, these are usually proteins from the surface spikes.[38] One of the challenges is to find a target unique to SARS-CoV-2.[39]

Antigen tests may be one way to scale up testing to much greater levels.[38] Isothermal nucleic acid amplification tests can process only one sample at a time per machine. RT-PCR tests are accurate but require too much time, energy and trained personnel to run the tests.[38] "There will never be the ability on a [PCR] test to do 300 million tests a day or to test everybody before they go to work or to school," Deborah Birx, head of the White House Coronavirus Task Force, said on 17 April 2020. "But there might be with the antigen test."[40]

A nasopharyngeal swab is exposed to paper strips containing artificial antibodies designed to bind to coronavirus antigens. Antigens bind to the strips and give a visual readout. The process takes less than 30 minutes, can deliver results at point of care, and does not require expensive equipment or extensive training.[38]

Swabs of respiratory viruses often lack enough antigen material to be detectable.[39] This is especially true for asymptomatic patients who have little if any nasal discharge. Viral proteins are not amplified in an antigen test.[38][41] According to the WHO the sensitivity of similar antigen tests for respiratory diseases like the flu ranges between 34% and 80%. "Based on this information, half or more of COVID-19 infected patients might be missed by such tests, depending on the group of patients tested," the WHO said. Many scientists doubt whether an antigen test can be made reliable enough in time to be useful against COVID-19.[41] According to the FDA, positive results from antigen tests are highly accurate, but there is a higher chance of false negatives, so negative results do not rule out infection. Therefore, negative results from an antigen test may need to be confirmed with a PCR test.[42]

Imaging[]

Typical visible features on CT initially include bilateral multilobar ground-glass opacities with a peripheral or posterior distribution.[43] Subpleural dominance, crazy paving, and consolidation may develop as the disease evolves.[43][44] Chest CT scans and chest x-rays are not recommended for diagnosing COVID-19. Radiologic findings in COVID-19 lack specificity.[45][43]

Antibody tests[]

Machine used to analyze blood samples
Table showing amounts of IgG and IgM antibodies detected in sample
Left: Automated analyzer for immunoassays, used, for example, to find SARS-CoV-2 antibodies. Right: Example of quantitative results for SARS-CoV-2 antibody test.

Blood tests (serology tests) may be able to identify once-infected people who have recovered,[46] however the timing of when people are tested is important.[47] SARS-CoV-2 antibodies' potency and protective period are unknown.[4][48] The potential role of antibody testing for determining if a person is immune to COVID-19 is not clear and the ability to detect SARS-COV-2 antibodies in people recovering from an infection, people who are asymptomatic, and those who had mild symptoms needs further research.[47]

Part of the immune system's response to infection is the production of antibodies, including IgM and IgG. According to the FDA, IgM antibodies to SARS-CoV-2 are generally detectable several days after initial infection, although levels over the course of infection and beyond are not well characterized.[49] SARS-CoV-2 IgG antibodies generally become detectable 10–14 days after infection, sometimes earlier, and normally peak around 28 days after infection onset.[50][51] Antibodies emerge too late to serve as acute infection markers and only 30% of people who are COVID-19 positive were found to have detectable antibodies on day 7 of their infection.[47] Antibodies for some diseases persist in the bloodstream for many years, while others quickly fade away.[38]

Types[]

Rapid diagnostic test (RDT)[]

RDTs typically use a small, portable, positive/negative lateral flow assay that can be executed at point of care. RDTs may process blood samples, saliva samples, or nasal swab fluids. RDTs produce colored lines to indicate positive or negative results.[52]

Enzyme-linked immunosorbent assay (ELISA)[]

ELISAs can be qualitative or quantitative and generally require a lab. These tests usually use whole blood, plasma, or serum samples. A plate is coated with a viral protein, such as a SARS-CoV-2 spike protein. Samples are incubated with the protein, allowing any antibodies to bind to it. The antibody-protein complex can then be detected with another wash of antibodies that produce a color/fluorescent readout.[52]

Neutralization assay[]

Neutralization assays assess whether sample antibodies prevent viral infection in test cells. These tests sample blood, plasma or serum. The test cultures cells that allow viral reproduction (e.g., VeroE6 cells). By varying antibody concentrations, researchers can visualize and quantify how many test antibodies block virus replication.[52]

Chemiluminescent immunoassay[]

Chemiluminescent immunoassays are quantitative lab tests. They sample blood, plasma, or serum. Samples are mixed with a known viral protein, buffer reagents and specific, enzyme-labeled antibodies. The result is luminescent. A chemiluminescent microparticle immunoassay uses magnetic, protein-coated microparticles. Antibodies react to the viral protein, forming a complex. Secondary enzyme-labeled antibodies are added and bind to these complexes. The resulting chemical reaction produces light. The radiance is used to calculate the number of antibodies. This test can identify multiple types of antibodies, including IgG, IgM, and IgA.[52]

Neutralizing vs binding antibodies[]

Most if not all large scale COVID-19 antibody testing looks for binding antibodies only and does not measure the more important neutralizing antibodies (NAb).[53][54][55] A NAb is an antibody that defends a cell from an infectious particle by neutralizing its biological effects. Neutralization renders the particle no longer infectious or pathogenic.[56] A binding antibody binds to the pathogen but the pathogen remains infective; the purpose can be to flag the pathogen for destruction by the immune system.[57] It may even enhance infectivity by interacting with receptors on macrophages.[58] Since most COVID-19 antibody tests return a positive result if they find only binding antibodies, these tests cannot indicate that the subject has generated protective NAbs that protect against re-infection.[54][55]

It is expected that binding antibodies imply the presence of NAbs[55] and for many viral diseases total antibody responses correlate somewhat with NAb responses[59] but this is not established for COVID-19. A study of 175 recovered patients in China who experienced mild symptoms reported that 10 individuals had no detectable NAbs at discharge, or thereafter. How these patients recovered without the help of NAbs and whether they were at risk of re-infection was not addressed.[54] An additional source of uncertainty is that even if NAbs are present, viruses such as HIV can evade NAb responses.[53]

Studies have indicated that NAbs to the original SARS virus (the predecessor to the current SARS-CoV-2) can remain active for two years[60] and are gone after six years.[61] Nevertheless, memory cells including Memory B cells and Memory T cells[62] can last much longer and may have the ability to reduce reinfection severity.[61]

Other tests[]

Following recovery, many patients no longer have detectable viral RNA in upper respiratory specimens. Among those who do, RNA concentrations three days following recovery are generally below the range in which replication-competent virus has been reliably isolated.[63]

No clear correlation has been described between length of illness and duration of post-recovery shedding of viral RNA in upper respiratory specimens.[64]

Infectivity[]

Infectivity is indicated by the basic reproduction number (R0, pronounced "R naught") of the disease.[65] SARS-CoV-2 is estimated to have an R0 of 2.2 to 2.5.[66][67] This means that in a population where all individuals are susceptible to infection, each infected person is expected to infect 2.2 to 2.5 others in the absence of interventions.[68] R0 can vary according factors such as geography, population demographics and density.[69] In New York state R0 was estimated to be 3.4 to 3.8.[70]

On average, an infected person begins showing symptoms five days after infection (the "incubation period") and can infect others beginning two to three days before that.[66][71] One study reported that 44% of viral transmissions occur within this period.[66][72] According to CDC, a significant number of infected people who never show symptoms are nevertheless contagious.[72][67] In vitro studies have not found replication-competent virus after 9 days from infection.[73] The statistically estimated likelihood of recovering replication-competent virus approaches zero by 10 days.[74]

Infectious virus has not been cultured from urine or reliably cultured from feces;[75] these potential sources pose minimal if any risk of transmitting infection and any risk can be sufficiently mitigated by good hand hygiene.

Patterns and duration of illness and infectivity have not been fully described. However, available data indicate that SARS-CoV-2 RNA shedding in upper respiratory specimens declines after symptom onset. At 10 days recovery of replication-competent virus in viral culture (as a proxy of the presence of infectious virus) approaches zero. Although patients may produce PCR-positive specimens for up to six weeks,[76] it remains unknown whether these samples hold infectious virus. After clinical recovery, many patients do not continue to shed. Among recovered patients with detectable RNA in upper respiratory specimens, concentrations after three days are generally below levels where virus has been reliably cultured. These data were generated from adults across a variety of age groups and with varying severity of illness. Data from children and infants were not available.[73]

History[]

Timeline of total number of tests in different countries[77]

January[]

Scientists from China first released information on the viral genome on 11 January 2020,[78][79] sending multiple genomic sequences to GISAID, an indispensable mechanism for sharing influenza genetic sequence data.[80] That day the Malaysian Institute for Medical Research (IMR) produced "primers and probes" specific to a SARS-CoV-2 RT-PCR test.[81] The IMR's materials were used to diagnose Malaysia's first patient on 24 January.[82] BGI Group was one of the first companies to receive emergency use approval from China's National Medical Products Administration for a nucleic acid test.[83]

Public Health England announced a test on the 10th,[84] using a real-time RT-PCR (RdRp gene) assay based on oral swabs.[85] The test detected the presence of any type of coronavirus, including specifically identifying SARS-CoV-2. It was rolled out to twelve laboratories across the United Kingdom on 10 February.[86]

The first case in South Korea was confirmed on 19 January.[87]

The German nucleic acid testing protocol was published on the 17th. Another early PCR test was developed by Charité University hospital in Berlin, working with academic collaborators in Europe and Hong Kong, and published on the 23rd. It used rtRT-PCR, and formed the basis of 250,000 kits distributed by the World Health Organization (WHO).[88]

In the US, the CDC developed its SARS-CoV-2 Real Time PCR Diagnostic Panel.[89] The protocol became available on the 28th.[90] One of three tests in early kits failed due to faulty reagents.

In Russia, the first COVID‑19 test was developed by the State Research Center of Virology and Biotechnology VECTOR. Production began on 24 January.[91]

February[]

CDC refused to let other labs process tests that month; allowing an average of fewer than 100 samples/day to be processed. Tests using two components were not determined to be reliable until the 28th, and only then were state and local laboratories permitted to begin testing.[92] The test was approved by the FDA under an EUA.[citation needed]South Korean company Kogenebiotech's clinical grade, nucleic acid test (PowerChek Coronavirus) was approved by Korea Centers for Disease Control and Prevention (KCDC) on 4 February.[93]

In Wuhan BGI opened a makeshift 2000-sq-meter emergency detection laboratory named "Huo-Yan" (Chinese: 火眼, "Fire Eye") on the 5th.[94][95] It processed more than 10,000 samples/day.[96][95] Construction required 5 days.[97] The Wuhan Laboratory was followed by Huo-Yan labs in Shenzhen, Tianjin, Beijing, and Shanghai, in a total of 12 cities across China.

On 11 February the test was approved by the Federal Service for Surveillance in Healthcare.[98]

March[]

By 4 March China reached 50,000 tests per day.[99]

On the 16th WHO called for ramping up testing programmes as the best way to slow the spread.[100][101]

Shortages of reagent and other supplies became a bottleneck for mass testing in the EU and UK[102] and the US.[103][104]

On 12 March, Mayo Clinic announced a nucleic acid test.[105]

Early in March, China reported accuracy problems with its PCR tests.[106] A study examined 1070 samples from 205 Wuhan patients and reported varied sensitivity according to the methods and location of sample collection. Samples from bronchoalveolar lavage fluid specimens returned the highest sensitivity.[107] The authors argued that CT scans showed even higher sensitivity.[108]

US commercial labs began testing in early March. As of the 5th LabCorp announced nationwide availability of COVID‑19 testing based on RT-PCR.[109] Quest Diagnostics made nationwide testing available as of 9 March.[110] US testing demand grew rapidly, causing backlogs of hundreds of thousands of tests at private US labs. Supplies of swabs and chemical reagents continued strained.[111] On 25 May, the US required each state to take responsibility for meeting its testing needs.[112] In March, the FDA issued EUAs for nucleic acid tests to Hologic (3/16),[113] Abbott Laboratories (3/18),[114] Thermo Fisher Scientific (3/19)[115] Cepheid (3/21)[116][117] and LabCorp (4/30).[114]

On 27 March the FDA issued an EUA for a test using Abbott Laboratories' ID Now assay.[118]

By 31 March United Arab Emirates was testing more of its population per head than any other country.[119] UAE implemented a combination of drive-through sample collection, and a mass-throughput laboratory from Group 42 and BGI. The lab conduced tens of thousands RT-PCR tests per day and was the first to be operational at that scale other than China.[120]

Several European countries initially conducted more tests than the US.[121][122] By 19 March drive-in tests were offered in several large cities.[123] As of 26 March, German Health Minister Jens Spahn estimated that Germany was conducting 200,000 tests per week.[124] As of the end of March at least 483,295 samples were tested and 33,491 (6.9%) had tested positive.[125]

80% of test kits that Czechia purchased from China gave wrong results.[126][127] Slovakia purchased 1.2 million antibody-based test kits from China that were found to be inaccurate.[128] China accused Czechia and Slovakia of incorrect use of those tests.[129] Ateş Kara of the Turkish Health Ministry said the test kits Turkey purchased from China had a "high error rate".[130][131]

Germany has a large medical diagnostics industry, with more than a hundred testing labs that provided the technology and infrastructure to enable rapid increases in testing. Costs are borne by insurance when the test is ordered by a physician.[132] According to the president of the Robert Koch Institute, as of 22 March, Germany had capacity for 160,000 tests per week.[133]

Spain purchased test kits from Chinese firm Shenzhen Bioeasy Biotechnology Co Ltd, but found that results were unacceptable. The maker explained that the incorrect results may stem from failure to collect samples or use the kits correctly. The Spanish ministry switched to another vendor, Shenzhen Bioeasy.[134]

By month end, testing had surpassed 200k/week.[135]

April[]

The FDA gave an EUA for the US' first antibody test on the 2nd.[136][48]

As of 7 April, WHO had accepted two diagnostic tests for procurement under the Emergency Use Listing procedure (EUL).[137]

On 13 April, Health Canada approved a nucleic acid test from Spartan Bioscience. Institutions may "test patients" with a handheld DNA analyzer "and receive results without having to send samples away to a [central] lab".[138][139]

By the start of April, the United Kingdom was delivering around 10,000 swab tests per day.[140] The British NHS announced that it was piloting a scheme to test suspected cases at home, to remove the risk of one patient infecting others at a hospital or disinfecting an ambulance used to transport a patient.[141]

The UK purchased 3.5 million antibody test kits from China, but in early April 2020 announced these were not usable.[142][143] On 21 April 2020, the Indian Council of Medical Research (ICMR) advised Indian states to stop using test kits purchased from China after receiving complaints from one state. Rajasthan health minister Raghu Sharma on 21 April said the kits gave only 5.4 percent accurate results.[144]

Antibody survey results found from 2% to 30% positive.[145] On preliminary data, WHO concluded that 2% to 3% of the world population had developed antibodies.[146]

By month end, testing had surpassed 750k/week.[135]

May[]

In May antibody tests were conducted on 5,603 major league baseball employees and 0.7% tested positive, showing that they had been infected. 70% of those who tested positive had had no symptoms.[147][148][149] The US was conducting an average of 2.5 million tests per week for the week ending 17 May. This grew to 3.2 million by 14 June.[150][151]

Attempts to culture virus from upper respiratory specimens were largely unsuccessful when viral burden is low but detectable (i.e., Ct values higher than 33-35).[73]

On 3 May, Roche received an EUA for a selective ELISA serology test.[152][153]

On 8 May, the FDA granted its first EUA for antigen test: "Sofia 2 SARS Antigen FIA" by Quidel Corp.[154][42]

The FDA announced on 14 May a review of 15 adverse event reports about the Abbott ID Now device for low sensitivity.[155]

On 21 May, researchers at Ben-Gurion University in Israel reported a one-minute coronavirus test with 90% accuracy, based on the "change in the resonance in the THz spectral range" shown by the coronavirus through THz spectroscopy.[156]

Nearly two million antibody tests imported into Australia and costing $20 million were declared unusable.[157][158][159]

In early May Harvard's Global Health Institute estimated that the US needed to test more than 900k per day.[160][161] Other recommendations ranged up to 23m per day.[162][163][164][165]

On 29 May Siemens received an EUA for its anti-spike RBD-targeting serology test that it believes detects neutralizing antibodies.[166]

By month end, testing had surpassed 1.4m/week.[135]

June[]

In early June, researchers announced a nucleic acid diagnostic test using reverse transcription-loop-mediated isothermal amplification (RT-LAMP), an existing technology used in pathogenic microorganism identification, genetically modified ingredients, tumor detection, and embryo sex identification. The test identified virus in samples of serum, urine, saliva, oropharyngeal swabs and nasopharyngeal swabs. Once commercialized the test has the potential to provide rapid (30-45 minute) diagnosis at point of care. The test was 100% selective and highly sensitive, detecting virus at a concentration of .06 fg/ml.[167]

As of 14 June 2020, the percentage testing positive in the US as a whole had fallen below 5%.[168] As of late June, test numbers crossed 600k/day.[150]

Testing protocols[]

A sample collection kiosk for COVID-19 testing in India

Drive-through testing[]

In drive-through testing, a healthcare professional takes a sample using appropriate precautions, such as wearing PPE.[169][170] Drive-through centers helped South Korea accelerate its testing program.[171]

Home collection[]

In Hong Kong test subjects can stay home and receive a specimen tube. They spit into it, return it and later get the result.[172]

Pooled testing[]

In Israel, researchers at Technion and Rambam Hospital developed a method for testing samples from 64 patients simultaneously, by pooling the samples and only testing further if the combined sample was positive.[173][174][175] Pool testing was then adopted in Israel, Germany, South Korea,[176] Nebraska,[177] China[178] and the Indian states of Uttar Pradesh,[179] West Bengal,[180] Punjab,[181] Chhattisgarh[182] and Maharashtra.[183]

Open source, multiplexed designs released by Origami Assays can test as many as 1122 patient samples using only 93 assays.[184] These balanced designs can be run in small laboratories without robotic liquid handlers.

Multi-tiered testing[]

One study proposed a rapid immune response assay as a screening test, with a confirmatory nucleic acid test for diagnosis, followed by a rapid antibody test to determine course of action and assess population exposure/herd immunity.[185]

Required volume[]

Required testing levels are a function of disease spread. The more the cases, the more tests are needed to manage the outbreak. COVID-19 tends to grow exponentially at the beginning of an outbreak, meaning that the number of required tests initially also grows exponentially. If properly targeted testing grows more rapidly than cases, it can be contained.

WHO recommends increasing testing until fewer than 10% are positive in any given jurisdiction.[186]

United States[]

Number of tests done per day in the US.
Blue: CDC lab
Orange: Public health lab
Gray: Data incomplete due to reporting lag
Not shown: Testing at private labs; total exceeded 100,000 per day by 27 March.[187]

Economist Paul Romer reported that the US has the technical capacity to scale up to 20 million tests per day, which is his estimate of the scale needed to fully remobilize the economy.[163] The Edmond J. Safra Center for Ethics estimated on 4 April that this capacity could be available by late July.[188] Romer pointed to single-molecule real-time sequencing equipment from Pacific Biosciences[189][163] and to the Ion Torrent Next-Generation Sequencing equipment from ThermoFisher Scientific.[190][163] According to Romer, "Recent research papers suggest that any one of these has the potential to scale up to millions of tests per day." This plan requires removing regulatory hurdles. Romer estimated that $100 billion would cover the costs.[163]

Romer also claimed that high test accuracy is not required if tests are administered frequently enough. He ran model simulations in which 7% of the population is tested every day using a test with a 20% false negative rate and a 1% false positive rate. The average person would be tested roughly every two weeks. Those who tested positive would go into quarantine. Romer's simulation indicated that the fraction of the population that is infected at any given time (known as the attack rate) peaks reaches roughly 8% in about thirty days before gradually declining, in most runs reaching zero at 500 days, with cumulative prevalence remaining below 20%.[191]

Available tests[]

A temporary drive-in testing site for COVID-19 set up with tents in a parking lot

Countries around the world developed tests independently and in partnership with others.

Nucleic acid tests[]

Tests developed in China, France, Germany, Hong Kong, Japan, the United Kingdom, and the US targeted different parts of the viral genome. WHO adopted the German system for manufacturing kits sent to low-income countries without the resources to develop their own.

PowerChek Coronavirus looks for the "E" gene shared by all beta coronaviruses, and the RdRp gene specific to SARS-CoV-2.[192]

US President Donald Trump displays a COVID-19 testing kit from Abbott Laboratories in March 2020.

Abbott Laboratories' ID Now nucleic acid test uses isothermal amplification technology.[118] The assay amplifies a unique region of the virus's RdRp gene; the resulting copies are then detected with "fluorescently-labeled molecular beacons".[193] The test kit uses the company's "toaster-size" ID Now device, which is widely deployed in the US.[194] The device can be used in laboratories or in point of care settings, and provides results in 13 minutes or less.[193]

Primerdesign offers its Genesig Real-Time PCR Coronavirus (COVID‑19). Cobas SARS-CoV-2 Qualitative assay runs on the Cobas® 6800/8800 Systems by Roche Molecular Systems. They are offered by the United Nations and other procurement agencies.

Antigen tests[]

Quidel's "Sofia 2 SARS Antigen FIA"[154][42] is a lateral flow test that uses monoclonal antibodies to detect the virus's nucleocapsid (N) protein.[195] The result is read out by the company's Sofia 2 device using immunofluorescence.[195] The test is simpler and cheaper but less accurate than nucleic acid tests. It can be deployed in laboratories or at point of care and gives results in 15 minutes.[154] A false negative result occurs if the sample's antigen level is positive but below the test's detection limit, requiring confirmation with a nucleic acid test.[195]

Serology (antibody) tests[]

Antibodies are usually detectable 14 days after the onset of the infection. Multiple jurisdictions survey their populations using these tests.[196][197] The test requires a blood draw.

Private US labs including Quest Diagnostics and LabCorp offer antibody testing upon request.[198]

Antibody tests are available in various European countries.[199] Quotient Limited developed a CE marked COVID-19 antibody test. [200][201][202]

Roche offers a selective ELISA serology test.[203]

Accuracy[]

Accuracy is measured in terms of specificity and selectivity. Test errors can be false positives (the test is positive, but the virus is not present) or false negatives, (the test is negative, but the virus is present).[204]

Sensitivity and specificity[]

Sensitivity indicates whether the test accurately identifies whether the virus is present. Each test requires a minimum level of viral load in order to produce a positive result. A 90% sensitive test will correctly identify 90% of infections, missing the other 10% (a false negative). Even relatively high sensitivity rates can produce high rates of false negatives in populations with low incidence rates.[204]

Specificity indicates how well-targeted the test is to the virus in question. Highly specific tests pick up only the virus in question. Non-selective tests pick up other viruses as well. A 90% specific test will correctly identify 90% of those who are uninfected, leaving 10% with a false positive result.[204]

Low-specificity tests have a low positive predictive value (PPV) when prevalence is low. For example, suppose incidence is 5%. Testing 100 people at random using a test that has a specificity of 95% would yield on average 5 people who are actually negative who would incorrectly test positive. Since 5% of the subjects actually are positive, another five would also test positive correctly, totaling 10 positive results. Thus, the PPV is 50%,[205] an outcome no different from a coin toss. In this situation retesting those with a positive result increases the PPV to 94.5%, meaning that only 4.5% of the second tests would return the incorrect result, on average less than 1 incorrect result.[206]

Causes of test error[]

Improper sample collection, exemplified by failure to acquire enough sample and failure to insert a swab deep into the nose. This results in insufficient viral load, one cause of low clinical sensitivity.

The time course of infection also affects accuracy. Samples may be collected before the virus has had a chance to establish itself or after the body has stopped its progress and begun to eliminate it.

Improper storage for too long a time can cause RNA breakdown and lead to wrong results as viral particles disintegrate.[207]

Improper design and manufacture can yield inaccurate results. Millions of tests made in China were rejected by various countries throughout the period of March 2020 through May 2020.

Test makers typically report the accuracy levels of their tests when seeking approval from authorities. In some jurisdictions, these results are cross-validated by additional assessments. Reported results may not be achieved in clinical settings due to such operational inconsistencies.

PCR-based test[]

Detection of SARS-CoV-2 by nasal swab over six weeks in patients who experienced mild to moderate illness

RT-PCR is the most accurate diagnostic test.[106] It typically has high sensitivity and specificity in a laboratory setting: however, in one study sensitivity dropped to 66-88% clinically.[208]

In one study sensitivity was highest at week one (100%), followed by 89.3%, 66.1%, 32.1%, 5.4% and zero by week six.[209][210]

The location of sample collection impact on sensitivity for COVID-19 in 205 Wuhan patients[107]
Samples from ... Positive rate
Bronchoalveolar lavage fluid specimens 93% (n=14)
Sputum 72% (n=75)
Nasal swabs 63% (n=5)
Fibrobronchoscope brush biopsy 46% (6/13)
Pharyngeal swabs 32% (n=126)
Feces 29% (n=44)
Blood 1% (n=3)

A Dutch CDC-led laboratory investigation compared 7 PCR kits.[211] Test kits made by BGI, R-Biopharm AG, BGI, KH Medical and Seegene showed high sensitivity.[212]

High sensitivity kits are recommended to assess people without symptoms, while lower sensitivity tests are adequate when diagnosing symptomatic patients.[211]

Isothermal nucleic amplification test[]

One study reported that the ID Now COVID-19 test showed sensitivity of 85.2%. Abbott responded that the issue could have been caused by analysis delays.[213] Another study rejected the test in their clinical setting because of this low sensitivity.[214]

Confirmatory testing[]

The WHO recommends countries that do not have testing capacity and national laboratories with limited experience on COVID‑19 send their first five positives and the first ten negative COVID‑19 samples to one of the 16 WHO reference laboratories for confirmatory testing.[215][216] Out of the sixteen reference laboratories, seven are in Asia, five in Europe, two in Africa, one in North America and one in Australia.[217]

National responses[]

Iceland[]

Iceland[218] managed the pandemic with aggressive contact tracing, inbound travel restrictions, testing, and quarantining, but with less aggressive lock-downs.

India[]

Italy[]

Researchers tested the entire population of , the site of Italy's first COVID‑19 death. They tested about 3,400 people twice, at an interval of ten days. About half the people testing positive had no symptoms. All discovered cases were quarantined. Along with restricting travel to the commune, new infections were completely eliminated.[219]

Japan[]

Unlike other Asian countries, Japan did not experience a pandemic of SARS or MERS, so the country's PCR testing system was not well developed.[220][221] Japan preferentially tested patients with severe illness and their close contacts at the beginning. Japan's Novel Coronavirus Expert Meeting chose cluster measures to identify infections clusters.[220][221] The Expert Meeting analyzed the outbreak from Wuhan and identified conditions leading to clusters (closed spaces, crowded spaces and close-contact), and asked people to avoid them.[221][222]

In January, contact tracers took action shortly after the first infection was found. Only administrative tests were carried out at first, until insurance began covering PCR tests on 6 March. Private companies began to test, and the test system gradually expanded.[220][223]

On 3 April, those with positive tests were legally permitted to recuperate at home or in a hotel if they had asymptomatic or mild illness, ending the hospital bed shortage.[224] The first wave (from China) was contained,[225] but a second wave (caused by returnees from Europe and the US) in mid-March led to spreading infection in April.[221] On 7 April, Japan declared a state of emergency, (less strict than a lockdown, because it did not block cities or restrict outings).[221][224][226] On 13 May, antigen test kits became covered by insurance, and were combined with a PCR test for diagnosis.[227][228]

Japan's PCR test count per capita remained far smaller than in some other countries even though its positive test rate was lower. Excess mortality was observed in March.[222][failed verification][226][failed verification][229] The Expert Meeting stated, "The Japanese health care system originally carries out pneumonia surveillance, allowing it to detect most of the severely ill patients who develop pneumonia. There are a large number of CT scanners in Japan and they have spread to small hospitals all over the country, so pneumonia patients are rarely missed. In that sense, it meets the same standards as other countries that mainly carry out PCR tests."[222][229] The group recommended using CT scans data and doctor's findings for diagnosis.[230][231] On the Diamond Princess cruise ship, many people who initially tested negative later tested positive. Half of coronavirus-positives there who remained mild or asymptomatic had pneumonia findings on CT scans and their CT image showed a frosted glass shadow that is characteristic of infection.[232][233]

As of July 18, Japan's daily PCR testing capacity was about 32,000, more than three times the 10,000 cases as of April. When the antigen test is added to it, the number is about 58,000. The number of tests per 1,000 people in the United States is about 27 times that of Japan, the UK is 20 times, Italy is 8 times, and South Korea is twice (as of July 26).[234][235][236] The number of those infected with coronavirus and inpatients has increased in July, but the number of serious cases has not increased. This is thought to be due to the proper testing of those infected in July compared to those in April. In April, the number of tests could not catch up with the increase in the number of infected people, and the test standards were strict, so the test positive rate exceeded 30% at the peak. It means that there were quite a few cases where the those infected was not PCR tested. It is thought that the severe case was preferentially tested though there were a lot of mild cases and asymptomatic carriers mainly in the young during the first wave. In other words, it became possible to grasp the actual situation of infection much better than before by strengthening the testing system.[237] At the end of July, accommodation facilities for mild and asymptomatic carriers became full, and the authorities requested hospitals to prepare beds for the mild. However, it became difficult to treat patients with other illnesses and to maintain the ICU system including the staff due to the occupation of hospital beds by patients with mild symptoms.[238][239][240]

Russia[]

On 27 April, Russia tested 3 million people and had 183,000 positive results.[241] On 28 April Anna Popova, head of Federal Service for Surveillance in Healthcare (Roszdravnadzor) stated that 506 laboratories were testing; that 45% of those who tested positive had no symptoms; that 5% of patients had a severe form; and 40% of infections were from family members. Illness improved from six days to one day after symptoms appeared. Antibody testing was carried out on 3,200 Moscow doctors, finding 20% immunity.[242]

Singapore[]

With contact tracing, inbound travel restrictions, testing, and quarantining, Singapore arrested the initial spread without complete lockdown.[243]

South Korea[]

South Korea's broad testing approach helped reduce spread. Testing capacity, largely in private sector labs, was built up over several years by the South Korean government in the early 2000s.[244]

The government exploited the resident registration number (RRN) system. Authorities mobilized young men who were eligible for military service as social service agents, security and public health doctors. Public health doctors were mainly dispatched to public health centers and life treatment centers where mildly ill patients were accommodated. They performed PCR tests and managed mild patients. Social service agents worked in pharmacies to fill staff shortages. Korea's 10k PCR tests per million residents was the world's highest as of 13 April rising to 20k by mid-June. Twenty-seven Korean companies exported test kits worth $48.6 million in March, and were asked to provide test kits or humanitarian assistance by more than 120 countries. Korean authorities set up a treatment center to isolate and manage patients with asymptomatic and minor illnesses in one facility in order to vacate hospital beds for the more severely ill.

Centers were sited mainly at national facilities and corporate training centers. The failure of Korea's MERS quarantine in May 2015 left Korea more prepared for COVID-19 than countries that did not face that pandemic. Then President Park Geun-hye allowed Korean CDC-approved private sector testing for infectious diseases in 2016. Korea already had a system for isolating, testing and treating infectious disease patients separately from others. Patients with respiratory illness but no epidemiological relevance were treated at the National Hospital, and those with epidemiological relevance were treated at selected clinics.[87][245][246][247][248][249][250][251][252]

Korea established a large scale drive-through/walk-through" test testing program. However, the most common method was “mobile examination”. In Daegu City, 54% of samples were collected by 23 March in home or hospital. Collecting samples door-to-door of avoided the risk of travel by possibly infected patients, but required additional staff. Korea solved the problem by drafting more than 2,700 public insurance doctors.[87][248][247]

The government disclosed personal information to the public via KCDC without patient consent. The authorities used digital surveillance to trace possible spread.[245][248][249][251][252][253][254][255][256] [257]

Taiwan[]

Health insurance IDs and national identification card numbers were used to trace contacts.[258][259][260][261]

United States[]

New York State[]

New York State's control measures consisted of PCR tests, stay-at-home measures and strengthening the healthcare system. On 29 February before its first case, the state allowed testing at the Wordsworth Center. They managed to convince the CDC to approve tests at state laboratories and the FDA to approve a test kit. As of 13 March the state was conducting more than 1,000 daily tests, growing to 10,000/day on 19 March. In April, the number exceeded 20,000. Many people queued at hospitals to get tested. On 21 March New York City health officials directed medical providers to test only those entering the hospital, for lack of PPE.[251][262][263][264][265]

USS Theodore Roosevelt[]

Following an outbreak, 94% of the 4,800 aircraft carrier crew were tested. Roughly 60 percent of the 600-plus sailors who tested positive were asymptomatic.[266] Five infected sailors who completed quarantine subsequently developed flu-like symptoms and again tested positive.[267]

Delayed testing[]

A shortage of trained medical laboratory scientists, assay reagents, analyzers, transport medium, and PPE coupled with high demand had limited initially limited the availability of testing and led to significantly increased turnaround times.

Testing statistics by country[]

Testing strategies vary by country and over time,[268] with some countries testing very widely,[7] while others have at times focused narrowly on only testing the seriously ill.[269] The country that tests only people showing symptoms will have a higher figure for "% (Confirmed cases as percentage of tested samples or tested cases)" than the country that also tests others.[270] If two countries are alike in every respect, including which people they test, the one that tests more people will have a higher "Confirmed / million people". Studies have also found that countries that test more, relative to the number of deaths, have lower estimated case fatality rates[8] and younger age distributions of cases.[10]

COVID-19 testing statistics by country
Country Date[a] Tested Units[b] Confirmed
(cases)
% Tested /
million
people
Confirmed /
million
people
Ref.
Afghanistan 11 August 97,199 samples 36,542 41.3 2,274 939 [271]
Albania 7 August 44,881 samples 6,151 13.7 15,676 2,148 [272]
Algeria 5 August 79,981 samples 32,499 40.6 1,834 745 [273]
Argentina 29 July 675,011 samples 173,355 25.7 14,875 3,820 [274]
Armenia 13 August 180,497 samples 41,023 22.7 61,149 13,898 [275]
Australia 13 August 5,041,344 samples 22,358 0.44 199,263 884 [276]
Austria 12 August 983,018 22,392 2.3 110,419 2,515 [277]
Azerbaijan 13 August 812,033 samples 33,915 4.2 82,040 3,426 [278]
Bahrain 12 August 933,762 samples 45,264 4.8 594,963 28,841 [279]
Bangladesh 29 July 1,164,195 samples 234,889 20.2 7,069 1,426 [280]
Barbados 30 July 10,881 143 1.3 37,910 498 [281]
Belarus 23 July 1,219,705 samples 66,688 5.5 128,501 7,026 [282]
Belgium 7 August 1,346,748 samples 72,016 5.3 116,948 6,254 [283]
Bhutan 7 August 55,354 samples 113 0.20 74,631 152 [284]
Bolivia 29 July 144,153 cases 73,534 51.0 12,614 6,434 [285]
Bosnia and Herzegovina 10 August 152,346 samples 14,498 9.5 44,526 4,237 [286]
Brazil 13 August 13,464,336 samples 3,224,876 24.0 64,071 15,346 [287][288]
Bulgaria 27 July 239,294 samples 10,427 4.4 34,431 1,500 [289]
Burkina Faso 29 July 17,400 samples 1,213 7.0 832 58 [290][291]
Cameroon 16 July 135,000 samples 16,157 12.0 5,086 609 [292]
Canada 12 August 4,581,083 samples 120,844 2.6 120,889 3,189 [293]
Chile 12 August 1,908,964 samples 378,168 19.8 100,097 19,829 [294]
China 31 July 160,000,000 samples 91,418 0.06 111,163 64 [295][296][297][298]
Colombia 13 August 2,063,332 samples 433,805 21.0 42,756 8,989 [299]
Costa Rica 7 August 102,257 samples 22,081 21.6 20,454 4,417 [300]
Croatia 5 August 124,383 cases 5,376 4.3 30,514 1,319 [301]
Cuba 28 July 256,996 samples 2,588 1.0 22,690 228 [302]
Cyprus[c] 12 August 243,405 samples 1,291 0.53 281,959 1,495 [303]
Czechia 5 August 722,003 samples 17,529 2.4 67,515 1,639 [304]
Denmark 12 August 1,874,640 samples 15,419 0.8 315,966 2,599 [305]
DR Congo 28 July 44,051 8,873 20.1 492 99 [306]
Ecuador 13 August 276,491 samples 98,343 35.6 16,184 5,756 [307]
Egypt 29 July 449,968 samples 93,356 20.7 4,496 933 [306]
El Salvador 30 July 236,501 samples 16,230 6.9 36,462 2,502 [308]
Estonia 26 July 116,915 samples 2,034 1.7 88,015 1,531 [309]
Ethiopia 19 July 331,366 samples 10,207 3.1 2,882 89 [310]
Finland 26 July 339,225 samples 7,393 2.2 61,196 1,334 [311]
France[d] 21 July 3,510,897 177,338 5.1 52,384 2,646 [312][313][314]
Germany 29 July 8,006,135 samples 206,926 2.6 96,286 2,489 [315]
Ghana 20 July 344,137 27,667 8.0 11,075 890 [273]
Greece 19 July 410,766 samples 4,007 0.98 38,145 372 [316]
Grenada 18 June 5,465 samples 24 0.44 49,034 215 [317]
Guinea 19 July 36,254 cases 6,544 18.1 2,761 498 [273]
Hungary 8 August 358,437 samples 4,653 1.3 37,104 482 [318]
Iceland 12 August 168,233 samples 1,972 1.2 461,849 5,414 [319]
India 13 August 26,845,688 samples 2,396,637 8.9 19,455 1,737 [320][321]
Indonesia 14 August 1,835,505 samples 135,123 7.4 6,702 493 [322]
Iran 7 August 2,637,575 samples 322,567 12.2 31,708 3,878 [323]
Iraq 20 July 809,522 samples 94,693 11.7 20,126 2,354 [324]
Ireland 10 August 670,771 samples 26,768 4.0 136,294 5,439 [325]
Israel 13 August 2,026,261 88,733 4.4 220,845 9,671 [326]
Italy 2 August 6,916,765 samples 248,070 3.6 114,593 4,110 [327]
Ivory Coast 28 July 87,683 15,713 17.9 3,324 596 [273]
Jamaica 28 July 37,210 samples 855 2.3 13,655 314 [328]
Japan 10 August 1,016,197 47,990 4.7 8,055 380 [329]
Kazakhstan 13 August 2,252,153 samples 101,372 4.5 120,736 5,434 [330]
Kenya 18 July 238,163 samples 12,750 5.4 5,007 268 [331]
Kosovo 9 June 17,199 samples 1,269 7.4 9,500 701 [332]
Kyrgyzstan 16 July 252,549 samples 12,498 4.9 39,526 1,956 [333][334]
Latvia 16 July 175,696 samples 1,179 0.67 91,510 614 [335]
Lebanon 29 July 286,340 4,205 1.5 41,952 616 [336]
Libya 5 August 55,899 cases 4,224 7.6 8,144 615 [306]
Lithuania 13 August 565,782 samples 2,330 0.41 202,475 834 [337]
Luxembourg[e] 10 August 661,307 samples 7,300 1.1 1,056,219 11,659 [338]
Madagascar 5 August 45,634 cases 12,222 26.8 1,738 465 [306]
Malawi 7 August 34,051 samples 4,575 13.4 1,780 239 [339]
Malaysia 26 July 937,645 cases 8,897 0.9 28,611 271 [340]
Maldives 7 August 86,651 samples 4,769 5.5 220,782 12,151 [341]
Malta 12 August 147,411 samples 1,190 0.81 298,669 2,411 [342]
Mauritius 2 June 120,358 samples 344 0.29 95,071 272 [343]
Mexico 29 July 863,536 cases 408,449 47.3 6,712 3,175 [344]
Moldova[f] 13 July 118,335 samples 19,382 16.4 44,817 7,341 [345]
Montenegro 4 August 24,469 cases 3,361 13.7 38,765 5,325 [346]
Morocco 7 August 1,405,159 cases 21,548 1.5 38,069 584 [347]
Mozambique 29 July 55,211 1,748 3.2 1,766 56 [348]
Myanmar 31 July 112,381 samples 361 0.32 2,065 6.6 [349]
Nepal 7 August 731,977 samples 21,750 3.0 26,053 774 [350]
Netherlands 4 August 668,851 cases 55,955 8.4 38,385 3,211 [351]
New Zealand 13 August 508,711 samples 1,239 0.24 102,077 249 [352]
Nigeria 30 July 276,053 samples 42,689 15.5 1,349 209 [353]
North Korea 19 June 922 cases 0 0 36 0 [354]
North Macedonia 8 August 113,537 samples 11,771 10.4 54,660 5,667 [355]
Northern Cyprus[g] 19 July 56,268 1702 3.02 172,601 5,221 [356]
Norway 21 July 407,311 cases 9,038 2.2 75,884 1,684 [357]
Oman 1 July 194,945 samples 41,194 21.1 41,947 8,864 [358]
Pakistan 28 July 1,931,102 samples 276,288 14.3 8,745 1,251 [359]
Palestine 9 August 216,765 samples 18,654 8.6 42,907 3,692 [360]
Panama 30 July 219,942 samples 64,191 29.2 52,657 15,368 [361]
Paraguay 30 July 125,361 samples 5,207 4.2 17,576 730 [362]
Peru 13 August 2,677,014 samples 507,996 19.0 81,556 15,476 [363]
Philippines 12 August 1,939,426 samples 143,749 7.4 19,206 1,424 [364]
Poland 25 July 2,095,222 samples 42,622 2.0 54,583 1,110 [365]
Portugal 13 August 1,783,267 samples 53,548 3.0 173,527 5,211 [366]
Qatar 12 August 533,995 samples 113,938 21.3 185,347 39,547 [367]
Romania 29 July 1,154,228 samples 48,235 4.2 59,491 2,486 [368]
Russia 8 August 30,640,020 samples 887,536 2.9 208,798 6,048 [369][370]
Rwanda 29 July 255,959 1,963 0.77 19,762 152 [371]
Saint Lucia 30 July 2,968 samples 25 0.8 16,318 137 [372]
Saudi Arabia 29 July 3,276,872 274,219 8.4 94,125 7,877 [373]
Senegal 26 July 104,061 9,681 9.3 6,564 611 [374]
Serbia 4 August 703,246 cases 26,738 3.8 100,986 3,840 [375]
Singapore 3 August 1,474,372 samples 53,051 3.6 258,498 9,301 [376][377]
Slovakia 12 August 284,111 samples 2,690 0.95 52,055 493 [378]
Slovenia 12 August 140,942 samples 2,332 1.7 67,306 1,114 [379]
South Africa 30 July 2,918,049 cases 482,169 16.5 49,201 8,130 [380]
South Korea 26 July 1,503,712 cases 14,150 0.94 29,080 274 [381]
Spain 13 August 7,472,031 samples 337,334 4.5 159,888 7,218 [382][383]
Sri Lanka 30 July 156,943 samples 2,810 1.8 7,242 130 [384]
Sudan 23 July 31,805 samples 11,302 35.5 725 258 [306]
Sweden 5 July 597,850 cases 72,693 12.2 57,889 7,039 [385]
Switzerland[h] 7 August 854,885 samples 37,169 4.4 96,316 4,213 [386]
Taiwan[i] 13 August 84,016 samples 481 0.57 3,559 20 [387]
Tanzania 6 June 2,680 509 19.0 45 8.5 [273]
Thailand 28 July 749,213 samples 3,356 0.48 10,126 48 [388]
Trinidad and Tobago 30 July 7,716 samples 326 4.2 5,657 239 [389]
Tunisia 5 August 102,041 cases 1,656 1.6 8,634 140 [390]
Turkey 9 August 5,263,816 samples 240,804 4.6 63,301 2,896 [391]
Uganda 19 July 238,709 samples 1,332 0.56 5,219 29 [392]
Ukraine 29 July 998,299 samples 67,597 6.8 23,752 1,608 [393]
United Arab Emirates 12 August 5,700,145 samples 63,212 1.1 593,805 6,585 [394]
United Kingdom 13 August 13,971,512 samples 313,798 2.2 206,845 4,646 [395]
United States 12 August 63,715,571 samples 5,172,216 8.1 192,502 15,627 [396][397]
Uruguay 30 July 110,951 samples 1,243 1.1 31,970 358 [398]
Uzbekistan 14 July 1,400,000 samples 13,872 0.99 41,132 408 [399]
Venezuela 17 July 1,420,066 samples 11,891 0.84 49,159 412 [400]
Vietnam 12 August 621,823 samples 883 0.34 2,644 8.9 [401]
Zimbabwe 30 July 129,899 samples 3,092 2.38 8,740 208 [402]
  1. ^ Local time.
  2. ^ For some countries it is unclear whether they report samples or cases. One person tested twice is recorded as one case and two samples.
  3. ^ Excluding Northern Cyprus.
  4. ^ Testing data from 4 May to 12 May is missing because of the transition to the new reporting system SI-DEP.
  5. ^ Data for residents only.
  6. ^ Excluding Transnistria.
  7. ^ Northern Cyprus is not recognized as a sovereign state by any country except Turkey.
  8. ^ Includes data for Liechtenstein.
  9. ^ Not a United Nations member.

See also[]

References[]

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