SARS-CoV-2 seroprevalence around the world: an updated systematic review and meta-analysis

Azami, Mobin; Moradi, Yousef; Moradkhani, Asra; Aghaei, Abbas

doi:10.1186/s40001-022-00710-2

European Journal of Medical Research

Table 1 Characteristics of included studies

From: SARS-CoV-2 seroprevalence around the world: an updated systematic review and meta-analysis

Authors (years) (R)	Country/WHO Regions	Study population	Sampling methods (random or non-random)	Study period	Type of detection methods	Race/ethnicity		Gender Male		Age		Seropositive people (based on months)	No. of people screened (sample size)	Seropositive people (total)
Herzog et al. [40]	Belgium (European Region)	Individuals aged 0–101 years	Random	March–July, 2020	ELISA			1799 (46.0%)		Highest % 60-70Y 507 (13.0%)		30 March–5 April 113	16,532	840
								1599 (47.1%)		10-20Y 442 (13.0%)		20-26April 204
								1587 (49.0%)		10-20Y 431 (13.3%)		18–26 May 224
								1425 (48.1%)		60-70Y 399 (13.5%)		8–13 June 163
								1471 (48.7%)		10-20Y 413 (13.7%)		29 June–4 July 136
Filho et al. [41]	Brazil (Region of the Americas)	Blood donors in Rio de Janeiro	Non-random	April, 2020	LFIA			1450		Highest % 30–49Y 1443 (3.7%)			2857	114 (4.0%)
Silveira et al. [42]	Brazil (region of the Americas)	Individuals in Canoas, Caxias do Sul, Ijuí, Passo Fundo, Pelotas, Porto Alegre, Santa Cruz do Sul, Santa Maria and Uruguaiana	Random (multi-stage sampling)	March–May, 2020	LFIA	White 76.0%		41.1%		Highest % 50–59 (17.1%)			4500	18
						Brown 15.3%
						Black 7.4%
						Other 1.3%
Torres et al. [43]	Chile (Region of the Americas)	Large School Community Subject	Non-random	April, 2020	LFIA			Students 54%		Mean 10.8			1009	100
Torres et al. [43]	Chile (Region of the Americas)	Large School Community Subject	Non-random	April, 2020	LFIA			Staff 27%		42.8			235	39
Chang et al. [44]	China (Western Pacific Region)	Blood donors in the cities of Wuhan, Shenzhen, and Shijiazhuang among 18–60-year-old adults	Non-random	January–April, 2020	VN	Wuhan Han: 17,126 (96.2)		11,077 (62.3)		Median 33			17,794	515
						Non-Han: 533 (3.0)
						Missing data: 135 (0.8)
						Shenzhen Han: 6519 (95.7)		4428 (65.0)		36			6810	3
						Non-Han: 274 (4.0)
						Missing data: 17 (0.2)
						Shijiazhuang Han: 13,414 (99.1)		9542 (70.5)		40			13,540	1
						Non-Han: 124 (0.9)
						Missing data: 2 (0.0)
To et al. [45]	China (Western Pacific Region)	In a hospital and university in Hong Kong	Random	December, 2019-Februray, 2020	ELISA					Median 59		April 12 to July 3, 2018: 295 (P7)	1214	29
												Jan 2 to June 28, 2019: 429 (17)
												July 2 to Dec 31, 2019: 401 (13)
												Jan 1 to Jan 31, 2020: 580 (15)
												Feb 1 to Feb 13, 2020: 233 (1)
Liang et al. [46]	China (Western Pacific Region)	Hospital visitors	Random	January–April, 2020	CLIA			Wuhan 4140 (50.0)		Median 55			8272	174
Liang et al. [46]	China (Western Pacific Region)	Hospital visitors	Random	January–April, 2020	CLIA			Guangzhou 4249 (48.3)		54			8782	53
Jerković et al. [47]	Croatia (European Region)	In Industry workers in Split-Dalmatia and Sˇibenik-Knin	Non-random	April, 2020	LFIA			Split-Dalmatia		Median 46			1316	13
Jerković et al. [47]	Croatia (European Region)	In Industry workers in Split-Dalmatia and Sˇibenik-Knin	Non-random	April, 2020	LFIA			Knin		45			178	6
Erikstrup et al. [48]	Denmark (European Region)	Blood donors aged 17–69 years	Non-random	April–May, 2020	LFIA			10,217		Highest % 5068			20,640	412
Petersen et al. [49]	Denmark (European Region)	Individuals In Faroe Islands	Random	April–May, 2020	ELISA			538 (50.2)		Median 42.1			1075	6
Ward et al. [50]	England (European Region)	ages 18 + years in England	Non-random	June–July, 2020	LFIA	White: 92,737		43,825		Highest % 45–54 20,634			99,908	5544
						Mixed: 1347
						Asian: 3658
						Black: 900
						Other: 762
Gallian et al. [51]	France (European Region)	In group O French blood donors	Non-random	March–April, 2020	VN			534		Median 41			998	27
Grzelak et al. [52]	France (European Region)	hospitalized patients, pauci-symptomatic individuals and blood donors	Random	March, 2020	ELISA			70 (35%)		Median 18			200	3
Fischer et al. [53]	Germany (European Region)	In blood donors located in three different federal states	Non-random	March–-June, 2020	ELISA								3186	29
Weis et al. [54]	Germany (European Region)	Individuals The CoNAN study	Non-random	May, 2020	ELISA			266 (47.3%)		Median 60			562	51
Bogogian-nidou et a. [55]	Greece (European Region)	Greece People by using the leftover sampling methodology	Random	March–April, 2020	CLIA			3001				March 5	6586	24
Bogogian-nidou et a. [55]	Greece (European Region)	Greece People by using the leftover sampling methodology	Random	March–April, 2020	CLIA			3001				April 19	6586	24
Merkely et al. [56]	Hungary (European Region)	Hungarian population included individuals aged 14 years or older, living in private households	Random	May, 2020	CLIA			4864 (46.4)		Mean 48.7			10,474	69
Shakiba et al. [57]	Iran (Eastern Mediterranean Region)	Individuals in Guilan province, Iran	Random	April, 2020	LFIA			270(49)		Highest % 18–60 343			551	117
Percivalle et al. [58]	Italy (European Region)	In blood donors from the Lodi Red Zone in Lombardy, Italy	Non-random	January–February, 2020	VN			272 (70%)		Median 43			390	91
Valenti et al. [59]	Italy (European Region)	Blood donors during the Covid-19 Milan outbreak	Random	February–April, 2020	LFIA			453		Mean 40.7			729	40
Fiore et al. [60]	Italy (European Region)	In healthy blood donors in South Eastern Italy	Random	May, 2020	CLIA			665		Highest % (46‐55) 246			904	9
Doi et al. [61]	Japan (Western Pacific Region)	Individuals in Kobe, Japan	Random	March–April, 2020	LFIA			486		Highest % 60–69 171			1000	33
Takita et al. [62]	Japan (Western Pacific Region)	Individuals in primary care clinics in Tokyo, Japan	Random	March–April, 2020	LFIA			461		Highest % 35–54 653			1071	41
Takita et al. [63]	Japan (Western Pacific Region)	Individuals at community clinics in Tokyo Authors:	Non-random	April–May, 2020	LFIA			87 (59%)		Highest % 40–49 58 (39)			147	7
Uyoga et al. [64]	Kenya (African Region)	In Kenyan blood donors	Random	April–June, 2020	ELISA			2540		Highest % 25 to 34 1242			3098	174
Song et al. [65]	Korea (Western Pacific Region)	Individuals without a history of the coronavirus disease infection in Daegu, Korea	Random	May–June, 2020	LFIA			99 (50%)		Highest % 40–59 89			198	15(7.6)
Kammon et al. [66]	Libya (African Region)	Among public community and health-care workers in Alzintan City of Libya	Random	April–May, 2020	LFIA			103					130	6
Snoeck et al. [67]	Luxembourg (European Region)	In the Luxembourgish population—the CON-VINCE study	Random	April–May, 2020	ELISA			911 (48.93)		Mean 47			1862	35
Sam et al. [68]	Malaysia (Western Pacific Region)	Individuals in Kuala Lumpur and Selangor, Malaysia	Random	January–June, 2020	VN			448					816	3
Pollán et al. [7]	Spain (European Region)	Spain population	Random	April–May, 2020	LFIA	Spanish: 57,858		29 349		Highest % 50–64 ≥ 65 15 094			61,075	3054
Pollán et al. [7]	Spain (European Region)	Spain population	Random	April–May, 2020	LFIA	Other: 2643		29 349		Highest % 50–64 ≥ 65 15 094			61,075	3054
Lundkvist et al. [69]	Sweden (European Region)	Two areas in Stockholm with different socio-economic conditions	Random	June, 2020	LFIA	Sweden as country of origin (%) 98.4		Djurgård-sstaden 42%		Mean 37			123	5
Lundkvist et al. [69]	Sweden (European Region)		Random	June, 2020	LFIA	1.1		Tensta 71%		50			90	27
Stringhini et al. [70]	Switzerland (European Region)	Former participants of the Bus Santé study and their household members	Random	April–May, 2020	ELISA			1312		Highest % 20–49 (n = 1096)		Week 1 (n = 341) 12	2766	219
												Week 2 (n = 469) 28
												Week 3 (n = 577) 61
												Week 4 (n = 604) 36
												Week 5 (n = 775) 82
Bendavid et al. [71]	USA (Region of the Americas)	Adults and children in Santa Clara County	Random	April, 2020	LFIA	Non-Hispanic 2116		1228 (36.9%)		Highest % 40–69 1706			3330	50
						White 623
						Hispanic 266
						Asian Other 306
Biggs et al. [72]	USA (Region of the Americas)	The Georgia shelter-in-place order for all residents (April 3–30)	Non-random	April–May, 2020	CLIA	White, non-Hispanic 329		317		Highest % 18–49 347			696	19
						Black, non-Hispanic 266
						Hispanic 44
						Asian/Pacific Islander, non-Hispanic 29
						Multiple race/ Other/ Unknown 28
Bryan et al. [73]	USA (Region of the Americas)	Individuals in Boise, Idaho	Random	April, 2020	CLIA			2,035 (41.9)		Highest % 1,142 (23.5)			4856	87
Dietrich et al. [74]	USA (Region of the Americas)	Children in Louisiana During the State Stay at Home Order	Random	March–May, 2020	ELISA	Black 347 (42.7)		403 (49.6%)		Median 11			812	62
						White 336 (41.4)
						Hispanic 43 (5.3)
						Other 86 (10.6)
Feehan et al. [38]	USA (Region of the Americas)	Individuals in New Orleans	Random	May, 2020	CLIA	White (1607)		38.2%		Mean 50.6			2640	181
						Black (828)
						Asian (130)
						Native American (14)
						Multiracial /other (58)
						Hispanic (293)
Havers et al. [39]	USA (Region of the Americas)	Individuals in 10 Sites in the United States	Random	March–May, 2020	ELISA			7178		Highest % ≥ 65 5802			16,025	515
McLaug-hlin et al. [75]	USA (Region of the Americas)	Individuals in a Ski Resort Community, Blaine County, Idaho, US	Random	May, 2020	CLIA	Hispanic or Latino 39		438		Highest % 50 to 59 225			917	208
McLaug-hlin et al. [75]	USA (Region of the Americas)		Random	May, 2020	CLIA	Non-Hispanic or Latino 735		438		Highest % 50 to 59 225			917	208
Menach-emi et al. [76]	USA (Region of the Americas)	Individuals In Indiana	Random	April, 2020	CLIA	White 3373 (92)		1,656 (45)		Highest % 40–59 1,328 (36)			3658	246
Menach-emi et al. [76]	USA (Region of the Americas)	Individuals In Indiana	Random	April, 2020	CLIA	Nonwhite 281 (8)		1,656 (45)		Highest % 40–59 1,328 (36)			3658	246
Ng et al. [77]	USA (Region of the Americas)	In donor and patient blood from the 2 San Francisco Bay Area	Random	March, 2020	CLIA								387	1
Rosenberg et al. [25]	USA (Region of the Americas)	Among a 15,101-patron convenience sample at 99 grocery stores in 26 counties throughout NYS	Random	April, 2020	MIA	Hispanic or Latino 17.4		47.6%		Highest % 55 + 36.1%			15,101	1887
						NH-White 58.0
						NH-Black/African American 13.9
						NH-Asian 8.6
						Multiracial /Other 2.1
Sood et al. [26]	USA (Region of the Americas)	Among adults in Los Angeles County, California	Random	April, 2020	LFIA	Hispanic 190		347		Highest % 35–54 475			863	35
						White (non-Hispanic) 497
						Black (non-Hispanic) 72
						Other 104
Akinbami et al. [78]	USA (Region of the Americas)	Among healthcare, first response, and public safety personnel, Detroit metropolitan area, Michigan	Non-random	May–June 2020	ELISA	No	% Seropositive	No	% Seropositive	Highest % No	% Seropositive		16,403	1132
						Non-Hispanic White 12,858	6.0	5,146 (31.4)	6.7	45–59 5,222 (31.9)	18–24 7.9
						Non-Hispanic Black 1,200	16.3
						Non-Hispanic Asian 1,097	7.3
						Hispanic 440	6.8
						Other‡ 404	7.2
						Declined to answer 398	7.0
Berardis et al. [79]	Belgium (European Region)	In a Belgian cohort of patients with cystic fibrosis	Non-random	April–May 2020	CLIA			76		Mean 24.9			149	4 (2.7%)
Borges et al. [80]	Brazil (Region of the Americas)	In an asymptomatic population in Sergipe	Random	May,2020	LFIA			1469 (48.2%)		Mean 39			3046	IgM 347
Borges et al. [80]	Brazil (Region of the Americas)	In an asymptomatic population in Sergipe	Random	May,2020	LFIA			1469 (48.2%)		Mean 39			3046	IgG 218
Borges et al. [81]	USA (Region of the Americas)	Among firefighters/paramedics of a US fire department	Non-random	April, 2020	LFIA	White 154 (78.2)		188 (93.5)		Highest % 41–50 67 (33.0)			203	18 (8.9)
						Black or African–American 9 (4.6)
						Multi- race 8 (4.1)
						Other 26 (13.2)
Clarke et al. [12]	United Kingdom (European Region)	In hemodialysis patients	Non-random	April–May, 2020	CLIA	+ (129)	− (227)	+	–	+ Median	–		356	129
						Black 18	28	82 (63.6)	144 (63.4)	65	68
						White 29	61
						Indo-Asian 60	94
						Other 22	44
De Carlo et al. [82]	Italy (European Region)	In healthcare professionals of a Southern Italy hospital	Non-random	March–May,2020	CLIA					Mean 46.5		March 4	3242	62
												April 9
												April28- May4 15
												May 35
Dingens et al. [83]	USA (Region of the Americas)	Among children visiting a hospital during the initial Seattle outbreak	Non-random	March–April, 2020	ELISA			541		Highest % ≥ 15 369			1076	10
Flannery et al. [84]	USA (Region of the Americas)	Among parturient women in Philadelphia	Non-random	April–June, 2020	ELISA	Black/Non-Hispanic 537		0		Median 31			1293	80
						White/Non-Hispanic 447
						Hispanic/Latino 125
						Asian 106
						Other/Unknown 78
Halatoko et al. [85]	Togo (African Region)	Among high-risk populations in Lome´ (Togo)	Random	April–May, 2020	ELISA			684 71.6%		Median 36			955	9
Hunter et al. [86]	USA (Region of the Americas)	Among healthcare workers with differing levels of coronavirus disease 2019 (Covid-19) patient exposure	Random	April–May, 2020	CLIA			30%		Mean 42.8			734	12
Khan et al. [87]	India ( South-East Asia Region)	Hospital visitors across District Srinagar	Non-random	July,2020	CLIA			1463		Highest % 30–49 1424			2906	111
Kobashi et al. [88]	Japan (Western Pacific Region)	Healthcare workers	Non-random	May,2020	CLIA			154 24.18%		Median 44			637	IgM 2
Kobashi et al. [88]	Japan (Western Pacific Region)	Healthcare workers	Non-random	May,2020	CLIA			154 24.18%		Median 44			637	IgG 6
Lastrucci et al. [89]	Italy (European Region)	In different essential activities during the general lock-down phase in the province of Prato (Tuscany, Italy)	Random	May,2020	ELISA			1532 (32.9%)		Median 49			4656	138 (3.0%)
Mahajan et al. [90]	USA (Region of the Americas)	Among Adults Living in Connecticut	Random	June, 2020	ELISA	Hispanic 49		244 47%		Mean 50.1			567	23 (4.1%)
						Non-Hispanic White 470
						Non-Hispanic Black 37
						Non-Hispanic Asian 9
						Non-Hispanic Other 5
Mansour et al. [91]	USA (Region of the Americas)	Among Healthcare Workers at a Tertiary Academic Hospital in New York City	Non-random	March–April, 2020	ELISA			111 (54%)		Mean 38			285	93
Mattern et al. [92]	France (European Region)	Circulation of SARS-CoV-2 in a maternity ward in an area that has been significantly affected	Non-random	May, 2020	CLIA			0		Mean 33			249	20
McDade et al. [93]	USA (Region of the Americas)	among household members of essential workers	Random	April–May, 2020	ELISA			105		Mean 37			232	30
Naranbhai et al. [94]	USA (Region of the Americas)	Chelsea residents, aged ≥ 18 years, with no current symptoms and no history of a positive SARS-CoV-2 PCR test	Non-random	April,2020	ELISA			120 (60%)		Median 46			200	63
Oliveira et al. [95]	Brazil (Region of the Americas)	In outpatients of a large public university hospital in Sao Paulo, Brazil	Random	June–August, 2020	ECLIA			156 (35.5)		Highest % 40–59			439	61
Pollán et al. [96]	Spain (European Region)	Spanish population	Random	April – May,2020	CLIA			29 349		Highest % 50–64 13 906			61,075	3054 (5%)
Psichogiou et al. [97]	Greece (European Region)	among health care workers in a country with low burden of Covid-19	Random	April- May, 2020	LFIA			453		Highest % 35–54 922			1495	15
Racine-Brzostek et al. [98]	USA (Region of the Americas)	in New York City Health Care Workers	Random	April–May, 2020	ELISA			834		Mean 37			2274	805
Shields et al. [99]	United Kingdom (European Region)	in healthcare workers	Random	April 2020	ELISA			128 (24.8%)		Median 42			516	126
Sood et al. [100]	USA (Region of the Americas)	Among adults in Los Angeles County, California	Random	April, 2020	LFIA	Hispanic 190		347		Highest % 35–54 475			863	100
						White (non-Hispanic) 497
						Black (non-Hispanic) 72
						Other 104
Tang et al. [101]	China (Western Pacific Region)	In hemodialysis centers	Non-random	December, 2019- March, 2020	ELISA			619 (60.3%)		Mean 60.3			1027	47
Younas et al. [21]	Pakistan ( Eastern Mediterranean Region)	Among healthy blood donors in Karachi, Pakistan	Random	June,2020	ECLIA			380		Mean 30.6			380	128(33.6%)
Anna et al. [24]	France (European Region)	Individuals in Paris	Non-random	March–April 2020	ELISA			418 22.6%		Mean 38			1847	183
Banjar et al. [102]	Saudi Arabia ( Eastern Mediterranean Region)	Among blood donors in the early months of the pandemic in Saudi Arabia	Random	May,2020	ECLIA			796		Mean 33.3			837	12
Coatsworth et al. [103]	Australia ( Western Pacific Region)	In elective surgical patients in Australia	Non-random	June–July 2020	ELISA	White 2607 (85.8)		1479 (48.7)		Mean 54			3037	15
						Asian 203 (6.7)
						ATSI 16 (0.5)
						Black/African 19 (0.6)
						Other 192 (6.3)
Ebinger et al. [104]	USA (Region of the Americas)	In healthcare workers	Random	May,2020	CLIA	(−) Asian 1809 (31)	( +) 57 (27)	1876 (32)	73 (34)	Mean (-) 41.6	Mean ( +) 38.5		6062	212
						Black 354 (6)	18 (8)
						White 2938 (50)	104 (49)
						Other 749 (13)	33 (16)
Kantele et al. [105]	Finland (European Region)	Among healthcare workers at Helsinki University Hospital, Finland	Non-random	March–April 2020	ELISA			187 (17.3%)		Median 38			1095	33
Ladoire et al. [106]	France (European Region)	Among the staff and patients of a French cancer center after first lockdown	Non-random	May–June 2020	ECLIA			Employees ( +) 2 (16.7%)	(−) 139 (21.4%) 649	Mean ( +) 35.3	38.6		663	12
Ladoire et al. [106]	France (European Region)		Non-random	May–June 2020	ECLIA			Patients ( +) 7 (41.2%)	299 (30.1%)	Mean ( +) 65.2	63.1		1011	17
Laursen et al. [107]	Sweden- Denmark (European Region)	Among Danish and Swedish Falck Emergency and Non-Emergency Healthcare Workers	Random	June–August 2020	LFIA	Swedish 1248		1939 (59.3)		Highest % 40–60 1732 (52.9)			3272	159 (4.9%)
Laursen et al. [107]	Sweden- Denmark (European Region)		Random	June–August 2020	LFIA	Danish 2024		1939 (59.3)		Highest % 40–60 1732 (52.9)			3272	159 (4.9%)
Lombardi et al. [108]	Italy (European Region)	Among healthcare workers of a large university hospital in Milan, Lombardy, Italy	Random	April–June 2020	CLIA			1232		Mean 44.8			4055	309
Moncunill et al. [109]	Spain (European Region)	Among health care workers in a Spanish hospital after 3 months of follow-up	Random	April–May 2020	ELISA			206		Mean 42			565	82
Pan et al. [110]	Taiwan ( Western Pacific Region)	Among healthcare workers in a tertiary care hospital in Taiwan	Random	July–Aug 2020	ELISA			70 36.8%		Mean 36.3			194	64
Pereckait et al. [111]	Lithuania (European Region)	In healthcare workers of Kaunas Hospitals	Random	June–September 2020	LFIA			63		Mean 43.4			432	5
McQuade et al. [112]	USA (Region of the Americas)	Among Outpatients in Virginia	Random	June–August, 2020	ELISA	Hispanic 396		1556 (33.3)		Mean 48.8			4675	101
McQuade et al. [112]	USA (Region of the Americas)	Among Outpatients in Virginia	Random	June–August, 2020	ELISA	Non-Hispanic 4279		1556 (33.3)		Mean 48.8			4675	101
Venugopal et al. [113]	USA (Region of the Americas)	Among health care workers in a New York City hospital	Random	March–May, 2020	ELISA	Hispanic 132 (28%)		149 (31%)		Highest % 20–39 230			478	130
						Black 87 (18%)
						Asian 114 (24%)
						Other race 30 (6%)
						Caucasian 115 (24%)
Malagón- Rojas et al. [114]	Colombia (Region of the Americas)	Healthcare workers in Colombia	Random	September–November 2020	CLIA	Afro- Colombian 216		788		36.45 ± 10.5			3296	1021
						White 995
						Indigenous 112
						Mestizo 2004
						Raizal 19
						Gipsy 6
Poustchi et al. [115]	Iran (Eastern Mediter-ranean Region)	High-risk occupational groups	Random	April 17 and June 2, 2020	ELISA			1795		Highest % 30–39 2995(33·6%)			3530	494
Poulikakos et al. [116]	England (European Region)	Healthcare workers in a tertiary center in North West	Random	May 2020	ELISA	Black or BAME 55 (19·6%)		205 (73%)					281	17
						did not declare ethnicity 25 (8·9%)
						DIPC 195 (69·4%)
Amendola et al. [117]	Italy (European Region)	Healthcare workers of the largest children hospital in Milan	Non-random	April 15, 2020	ELISA			108		Median 44			663	34
Brandstetter et al. [118]	Germany (European Region)	Hospital staff	Random	March 2020	ELISA			30		Highest % 36–50 72 (35.8)			201	31
Chibwana et al. [119]	Malawi (African Region)	Health Care Workers	Random	May 2020 to June 2020	ELISA			236		Median 31			500	84

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