Study characteristics
From 4024 citations, 150 studies (155 datasets), involving 44,473 PLWH, met the inclusion criteria for eligibility in a quantitative analysis of the prevalence of HIV–LT co-infection. Moreover, 65 studies, involving 17,705 PLWH, had data for HIV-AT co-infection (S2 Fig). Considering WHO regions, most studies were from Africa (45 for LT and 15 for AT), then the Eastern Mediterranean (23 for LT and 15 for AT); the fewest were in South America (nine for LT and four for AT). Supplementary Table 1 summarizes the characteristics of, and references to, included studies as well as geographic location of each.
Global prevalence of LT in PLWH
For the 155 data sets in 49 countries, 14,913 of 44,473 PLWH were diagnosed as having LT, resulting in an overall, pooled global prevalence of 37.4% (95% CI, 33.4–4.4) (Table 1; Fig. 1A), with evidence of heterogeneity among studies (I2 = 98.7%, P < 0.001). In WHO-regions, the pooled prevalences (in descending order, with a 95% CI) were 46.2% (37.7–54.7%) in Africa, 46.2% (29.6–62.6%) in South America, 45.8% (36.3–55.5%) in the Eastern Mediterranean region, 41.1% (33.0–49.4%) in Europe, 29.9% (22.0–38.3%) in South-East Asia, 25.5% (19.2–32.4%) in North America and 18.4% (12.4–25.3%) in the Western Pacific. For countries with two or more eligible studies, Ethiopia (80.5%), Ghana (70.6%), and Cameroon (54.5%) in Africa; Iran (45.7%) in the Middle East; France (72.5%) and Austria (57.3%) in Europe; Brazil (48.8%) in America and Indonesia (38.5%), Thailand (37.5%) and Malaysia (36.1%) in East Asia exhibited some of the highest seroprevalence rates (Table 1 and Fig. 1A). Moreover, we estimated that approximately 14,174,600 (12,658,600–15,690,600) PLWH worldwide were seropositive for LT. Our estimates demonstrated that countries in the African region, which has a large proportion of PLWH, also has the largest number of people with LT 11,873,400 (9,688,900–14,057,900), accounting for approximately 84% of cases of HIV-LT coinfection worldwide. Additional details pertaining to the prevalence and burden of LT in PLWH in WHO-regions and individual countries are given in Table 1 and Fig. 1A.
Table 1
Global, regional and national pooled prevalence of latent toxoplasmosis (LT) among people living with HIV (PLWH) (results from 155 datasets performed in 48 countries).
WHO regions/ country
|
Number datasets
|
Number of PLWH screened (total)
|
Number of PLWH with LT
|
Pooled prevalence (95% CI)
|
Estimated number of PLWH individuals*
|
Estimated number of PLWH with LT
|
Global
|
155
|
44473
|
14913
|
37.4 (33.4–41.4)
|
37,900,000
|
14,174,600 (12,658,600–15,690,600)
|
South Americas
|
9
|
2905
|
1270
|
46.2 (23.6–69.6)
|
1,900,000
|
877,800 (448,400–1,322,400)
|
Brazil
|
8
|
650
|
1203
|
48.8 (23.5–74.5)
|
900,000
|
439,200 (211,500–670,500)
|
Chile
|
1
|
255
|
67
|
26.3 (21.0–32.1)
|
71000
|
18,673 (14,910–22,791)
|
African region
|
49
|
9504
|
3967
|
46.2 (37.7–54.70)
|
25,700,000
|
11,873,400 (9,688,900–14,057,900)
|
Ethiopia
|
12
|
1778
|
1396
|
80.5 (66.3–91.6)
|
690,000
|
555,450 (457,740–632,040)
|
Nigeria
|
12
|
2149
|
709
|
30.3 (19.2–42.7)
|
1,900,000
|
575,700 (364,800–811,300)
|
Burkina Faso
|
5
|
2548
|
691
|
30.7 (25.5–36.2)
|
96,000
|
29,472 (24,480–34,752)
|
Cameroon
|
3
|
293
|
167
|
54.5 (37.5–71.1)
|
540,000
|
294,300 (202,500–383,940)
|
Ghana
|
2
|
519
|
365
|
70.6 (66.6–74.4)
|
330,000
|
232,980 (219,780–245,520)
|
Uganda
|
2
|
316
|
134
|
42.3 (36.9–47.8)
|
1,400,000
|
592,200 (516,600–669,200)
|
South Africa
|
2
|
407
|
62
|
13.5 (10.3–17.0)
|
7,700,000
|
1,039,000 (793,100–1,309,000)
|
Zambia
|
2
|
256
|
14
|
5.2 (2.7–8.4)
|
1,200,000
|
62,400 (32,400–100,800)
|
Mozambique
|
2
|
258
|
110
|
42.5 (36.5–47.7)
|
2,200,000
|
935,000 (803,000–1,049,400)
|
Tanzania
|
1
|
38
|
26
|
68.4 (51.3–82.5)
|
1,600,000
|
1,094,400 (820,800–1,320,000)
|
Canary island (Spain)
|
1
|
157
|
56
|
35.7 (28.2–43.7)
|
140,000
|
49,000 (39,480–61,180)
|
Botswana
|
1
|
46
|
3
|
6.5 (1.4–17.9)
|
370,000
|
24,050 (5,180–66,230)
|
Togo
|
1
|
56
|
14
|
25.0 (14.4–38.4)
|
110,000
|
27,500 (15,840–42,240)
|
Congo
|
1
|
375
|
75
|
22.0 (19.1–26.4)
|
89,000
|
19,580 (16,999–23,496)
|
Congo (Democratic Republic of the)
|
1
|
38
|
28
|
73.6 (52.5–94.6)
|
450,000
|
331,200 (236,250–425,700)
|
Central African Republic
|
1
|
270
|
117
|
43.3 (37.3–49.5)
|
110,000
|
47,630 (41,030–54,450)
|
Eastern Mediterranean
|
23
|
3151
|
1271
|
45.8 (36.3–55.5)
|
400,000
|
183,200 (145,200–222,000)
|
Iran
|
19
|
2886
|
1148
|
45.7 (35.3–56.3)
|
61,000
|
27,877 (21,533–34,343)
|
Saudi Arabia
|
1
|
50
|
15
|
30.0 (17.9–44.6)
|
13,000⁂
|
39,00 (2,327–5,798)
|
Bahrain
|
1
|
76
|
16
|
21.1 (12.5–31.9)
|
260⁂
|
55 (32–83)
|
Morocco
|
1
|
95
|
59
|
62.1 (51.6–71.9)
|
21,000
|
13,041 (10,836–15,099)
|
Sudan
|
1
|
44
|
33
|
75.0 (59.7–86.8)
|
59000
|
44,250 (35,223–51,212)
|
European region
|
20
|
8786
|
4109
|
41.1 (33.0–49.4)
|
2,500,000
|
1,027,500 (825,000–1,235,000)
|
Spain
|
4
|
1707
|
562
|
30.7 (9.4–57.7)
|
150,000
|
46,050 (14,100–86,550)
|
Turkey
|
2
|
788
|
352
|
45.2 (41.7–48.7)
|
14,800⁂
|
6,690 (6,172–7,207)
|
United Kingdom
|
2
|
609
|
164
|
26.9 (23.4–30.5)
|
101,600
|
27,330 (23,774–30,988)
|
France
|
2
|
1715
|
1237
|
72.5 (70.3–74.6)
|
180,000
|
130,500 (126,540–134,280)
|
Austria
|
2
|
659
|
377
|
57.3 (53.5–61.1)
|
9000⁂
|
5,157 (4,815–5,499)
|
Romania
|
2
|
224
|
69
|
30.5 (24.6–36.8)
|
18,000
|
5,490 (4,428–6,624)
|
Czech Republic
|
2
|
1302
|
20
|
40.0 (37.4–42.7)
|
4400
|
1,760 (1645–1879)
|
Croatia
|
1
|
166
|
86
|
51.8 (43.9–59.6)
|
1600
|
829 (702–953)
|
Germany
|
1
|
183
|
64
|
35.0 (28.1–42.4)
|
87,000
|
30,450 (24,447–36,888)
|
Denmark
|
1
|
503
|
223
|
44.3 (39.9–48.8)
|
6,200
|
2746 (2,474–3,025)
|
Switzerland
|
1
|
715
|
360
|
50.3 (46.6–54.1)
|
20,000
|
10,060 (9,320–10,820)
|
Serbia
|
1
|
288
|
127
|
44.1 (38.3–50.0)
|
3000
|
1,323 (1,149–1,500)
|
North America and the Caribbean
|
12
|
7202
|
1150
|
25.5 (19.2–32.4)
|
1,700,000
|
433,500 (326,400–550,800)
|
USA
|
8
|
5862
|
889
|
18.3 (13.3–23.9)
|
1,100,000
|
201,300 (146,300–262,900)
|
Mexico
|
2
|
187
|
91
|
10.6 (8.8–12.6)
|
230,000
|
24,380 (20,240–25,980)
|
Canada
|
1
|
1074
|
14
|
48.7 (41.5–55.9)
|
63,000
|
30,681 (26,148–35,217)
|
Cuba
|
1
|
79
|
56
|
70.9 (59.6–80.6)
|
31,000
|
21,979 (18,476–24,986)
|
South-East Asian Region
|
18
|
5232
|
1582
|
29.8 (22.0–38.3)
|
3,800,000
|
1,132,400 (836,000–1,455,400)
|
India
|
10
|
2773
|
532
|
24.1 (16.8–32.2)
|
2,200,000⁂
|
530,200 (369,600–708,400)
|
Indonesia
|
4
|
1131
|
447
|
38.5 (32.2–45.0)
|
640,000
|
246,400 (206,080–288,000)
|
Thailand
|
3
|
1328
|
603
|
37.5 (20.8–56.0)
|
480,000
|
180,000 (99,840–268,800)
|
Western Pacific Region
|
24
|
7630
|
1530
|
18.4 (12.4–25.3)
|
1,900,000
|
349,600 (235,600–480,700)
|
China
|
10
|
3768
|
598
|
12.2 (5.5–20.9)
|
900000⁂
|
109,800 (49,500–188,100)
|
Malaysia
|
6
|
1507
|
511
|
36.1 (18.4–56.1)
|
87,000
|
31,407 (16,008–48,807)
|
Japan
|
4
|
680
|
67
|
9.9 (6.4–14.0)
|
30,000
|
2,970 (1,920–4,200)
|
Taiwan
|
1
|
550
|
56
|
10.2 (7.8–13.0)
|
48,000
|
4,896 (3,744–6,240)
|
South-Korea
|
1
|
173
|
7
|
4.0 (1.6–8.2)
|
45,000
|
1,800 (720–3,690)
|
Singapore
|
1
|
771
|
183
|
23.7 (20.8–26.9)
|
7900
|
1,872 (1,643–2,125)
|
Papua New Guinea
|
1
|
181
|
108
|
59.7 (52.1–66.9)
|
45,000
|
26,865 (23,445–30,105)
|
Abbreviations: NA: not applicable |
WHO regions are sorted according to prevalence rates |
Countries are sorted according to number of studies included |
Subgroup and meta-regression analyses according to socio-demographic and study characteristics
In subgroup analyses, with respect to income level and HDI, the highest prevalence of LT was in low-income countries (58.2%, 46.2–69.8%) and the lowest prevalence was in high-income countries (28.0%, 21.3–35.2%). The pooled prevalence of LT in PLWH in countries with low, medium, high and very high levels of HDI were 51.9% (42.8–60.8%), 29.3% (20.9–38.4%), 38.0% (22.6–33.1%), and 27.6% (22.6–33.1%), respectively (Table 2). Meta-regression analyses revealed a significant decreasing trend in prevalence in countries with increasing per capita income (C = -2.97e − 06; P-value = 0.004) and HDI levels (C = -0.473; P-value < 0.001) (Fig. 2A and B). Studies that were performed after 2005 showed slightly higher prevalence rates than other periods, although this increasing trend (1980–2020) was non-significant in meta-regression analysis (C = 0.0016; P value = 0.46) (Table 2 and Fig. 2C). In subgroup analyses, according to type of study, the highest and lowest prevalence rates were estimated in case-control (40.4%, 30.7–50.6%) and retrospective cohorts (26.5%, 17.1–37.2%), respectively. Subgroup analysis based on diagnostic methods revealed the lowest (30.5%, 14.9–48.9%) and highest (57.2%, 47.0–67.1%) prevalences in studies that used the Sabin-Feldman (SFT) and immunofluorescence (IFAT) methods, respectively. The prevalence rate in studies using ELISA, the most commonly used method, was 35.5% (31.1–40.1%). More subgroup analyses and details are given in Table 2. With respect to age, prevalence rates of LT in PLWH < 20, 20–40, 40–60 and > 60 years were (13.8%, 11.8–15.7%), (39.5%, 38.7–40.4%), (46.3%, 44.9–47.7%) and (43.7%, 37.1–50.3%), respectively (Table 3). With respect to the number of CD4 + lymphocytes in patients, prevalence rates of LT in PLWH with CD4 + counts of < 200, 200–500 and > 500 were (18.4%, 16.8–20.0%), (33.8%, 32.6–34.9%) and (21.9%, 20.5–23.3%), respectively (Table 3).
Table 2
Prevalence of latent toxoplasmosis (LT) and acute toxoplasmosis (AT) in people living with HIV (PLWH) according to a priori defined subgroups
Variable/subgroups
|
Number datasets
|
Number of PLWH screened (total)
|
Number of PLWH with LT
|
Pooled prevalence (95% CI)
|
Number of PLWH with AT
|
Pooled prevalence (95% CI)
|
LT
|
AT
|
LT
|
AT
|
Income
|
|
|
|
|
|
|
|
|
Low
|
27
|
5
|
5950
|
973
|
2675
|
58.2 (46.2–69.8)
|
8
|
0.4 (0.0–1.9)
|
Lower middle
|
35
|
13
|
7168
|
3389
|
2350
|
34.5 (27.0–42.3)
|
72
|
1.8 (0.7–3.2)
|
Upper middle
|
55
|
28
|
13980
|
5764
|
4682
|
36.0 (29.2–43.1)
|
105
|
1.4 (0.7–2.3)
|
High
|
38
|
20
|
17375
|
7579
|
5206
|
28.0 (21.3–35.2)
|
104
|
1.2 (0.6–1.9)
|
HDI
|
|
|
|
|
|
|
|
|
Low
|
42
|
8
|
7969
|
1307
|
3533
|
51.9 (42.8–60.8)
|
23
|
1.4 (0.1–3.7)
|
Medium
|
22
|
12
|
5556
|
3462
|
1554
|
29.3 (20.9–38.4)
|
64
|
1.5 (0.6–2.6)
|
High
|
47
|
25
|
13405
|
6858
|
45269
|
38.0 (22.6–33.1)
|
109
|
1.3 (0.6–2.2)
|
Very high
|
44
|
21
|
17543
|
6078
|
4557
|
27.6 (22.6–33.1)
|
93
|
1.3 (0.7–2.0)
|
Type of study
|
|
|
|
|
|
|
|
|
Cross sectional
|
95
|
44
|
24576
|
8739
|
7941
|
38.7 (33.6–44.0)
|
148
|
1.2 (0.7–1.8)
|
Case-control
|
32
|
10
|
5204
|
1895
|
2059
|
40.4 (30.7–50.6)
|
36
|
2.6 (0.8–5.0)
|
Prospective cohort
|
9
|
4
|
3534
|
1591
|
1151
|
36.6 (19.1–56.1)
|
34
|
2.1 (1.1–3.4)
|
Retrospective cohort
|
19
|
8
|
11159
|
5480
|
3762
|
26.5 (17.1–37.2)
|
71
|
1.0 (0.3–1.0)
|
Acute toxoplasmosis criteria
|
|
|
|
|
|
|
|
|
IgG & IgM
|
NA
|
50
|
NA
|
9872
|
NA
|
NA
|
166
|
1.2 (0.7–1.8)
|
Seroconversion
|
NA
|
12
|
NA
|
6715
|
NA
|
NA
|
88
|
1.2 (0.8–1.7)
|
IgG avidity
|
NA
|
2
|
NA
|
961
|
NA
|
NA
|
28
|
1.7 (1.0–2.7)
|
Antigen detection
|
NA
|
2
|
NA
|
157
|
NA
|
NA
|
7
|
3.5 (1.0–7.2)
|
Year
|
|
|
|
|
|
|
|
|
< 2000
|
35
|
17
|
11920
|
5894
|
4282
|
37.5 (29.4–46.0)
|
82
|
1.2 (0.6–1.9)
|
2000–2005
|
14
|
3
|
6366
|
1095
|
1823
|
26.2 (17.3–36.2)
|
6
|
0.5 (0.0–1.6)
|
2006–2010
|
17
|
4
|
2893
|
726
|
803
|
28.7 (15.7–43.8)
|
5
|
0.4 (0.0–1.2)
|
2011–2015
|
49
|
16
|
12386
|
4212
|
4475
|
45.3 (37.4–53.3)
|
90
|
1.7 (0.7–3.2)
|
2016–2020
|
40
|
26
|
10908
|
5688
|
3530
|
35.6 (27.8–43.9)
|
106
|
1.5 (0.7–2.5)
|
Sample size
|
|
|
|
|
|
|
|
|
≤ 99
|
45
|
20
|
2987
|
1338
|
1269
|
41.5 (33.7–49.6)
|
55
|
2.9 (1.2–5.1)
|
100–300
|
65
|
27
|
11526
|
4782
|
4807
|
43.1 (36.3–50.1)
|
77
|
1.0 (0.4–1.8)
|
301–500
|
22
|
10
|
8372
|
4016
|
2067
|
22.0 (14.5–30.7)
|
72
|
1.6 (1.0–2.4)
|
501–1000
|
16
|
7
|
11132
|
4651
|
3530
|
29.9 (19.7–41.1)
|
57
|
0.9 (0.3–2.0)
|
> 1000
|
7
|
2
|
10456
|
2918
|
3241
|
29.8 (14.7–47.7)
|
28
|
1.0 (0.6–1.3)
|
Risk of bias (total number of item with “yes” answers per study)
|
|
|
|
|
|
|
|
|
Low
|
118
|
50
|
42227
|
16736
|
13984
|
36.1 (31.6–40.6)
|
249
|
1.2 (0.8–1.6)
|
Moderate
|
37
|
16
|
2246
|
969
|
967
|
41.8 (33.4–41.4)
|
40
|
2.8 (1.0–5.4)
|
Method
|
|
|
|
|
|
|
|
|
ELISA
|
125
|
NA
|
35286
|
NA
|
11736
|
35.5 (31.1–40.1)
|
NA
|
NA
|
IFAT
|
9
|
NA
|
2828
|
NA
|
1486
|
57.2 (47.0–67.1)
|
NA
|
NA
|
LAT
|
5
|
NA
|
658
|
NA
|
395
|
61.9 (40.9–80.8)
|
NA
|
NA
|
MEIA
|
5
|
NA
|
1631
|
NA
|
321
|
30.1 (14.3–48.8)
|
NA
|
NA
|
SFT
|
6
|
NA
|
3199
|
NA
|
706
|
30.5 (14.9–48.9)
|
NA
|
NA
|
Other (MAT, CFT, ELFA, DAT)
|
5
|
NA
|
871
|
NA
|
269
|
40.2 (15.4–68.0)
|
NA
|
NA
|
Table 3
Risk factors associated with Toxoplasma gondii seropositivity among people living with HIV (PLWH)
Variables (number of studies)
|
Number of PLWH
|
Number (%) of seropositive
|
Pooled prevalence (95% CI)
|
OR (95% CI)
|
Heterogeneity
|
Publication bias P value |t|
|
I2 (%)
|
|
Gender (34)
|
|
|
|
|
89.1
|
0.25
|
Female
|
5806
|
2106
|
35.16 (34.28, 36.03)
|
1
|
|
|
Male
|
7826
|
2363
|
29.44 (28.60, 30.28)
|
0.78 (0.55–1.12)
|
|
|
Residence (9)
|
|
|
|
|
36.9
|
0.44
|
Urban
|
1472
|
820
|
59.73 (57.61, 61.84)
|
1
|
|
|
Rural
|
283
|
166
|
67.29 (63.16, 71.42)
|
1.45 (0.76–2.75)
|
|
|
Close contact with dog (3)
|
|
|
|
|
90.1
|
0.98
|
No
|
531
|
141
|
17.47 (14.89, 20.05)
|
1
|
|
|
Yes
|
235
|
56
|
16.36 (12.46, 20.26)
|
2.69 (0.55–13.18)
|
|
|
Close contact with cats (15)
|
|
|
|
|
84.0
|
0.31
|
No
|
1753
|
919
|
76.52 (74.94, 78.10)
|
1
|
|
|
Yes
|
1039
|
611
|
75.39 (73.13, 77.64)
|
1.79 (0.91–3.50)
|
|
|
Contact with soil (5)
|
|
|
|
|
67.2
|
0.5
|
No
|
442
|
219
|
46.84 (43.18, 50.49)
|
1
|
|
|
Yes
|
316
|
236
|
83.92 (80.26, 87.58)
|
3.01 (1.50–6.04)
|
|
|
Consumption of raw meat (15)
|
|
|
|
|
78.5
|
0.88
|
No
|
1626
|
892
|
68.09 (66.65, 69.53)
|
1
|
|
|
Yes
|
1016
|
699
|
85.28 (83.54, 87.02)
|
2.01 (1.19–3.39)
|
|
|
Consumption of raw/unwashed vegetable (8)
|
|
|
|
|
13.7
|
0.26
|
No
|
493
|
411
|
88.79 (86.14, 91.43)
|
1
|
|
|
Yes
|
756
|
653
|
95.28 (93.82, 96.74)
|
1.04 (0.68–1.6)
|
|
|
Drinking untreated water (5)
|
|
|
|
|
45.5
|
0.19
|
No
|
835
|
612
|
82.19 (79.95, 84.44)
|
1
|
|
|
Yes
|
298
|
207
|
83.64 (80.24, 87.03)
|
1.19 (0.67–2.11)
|
|
|
Number of CD4 (29)
|
|
|
|
|
|
|
≥ 500
|
1733
|
440
|
18.48 (16.88, 20.09)
|
1
|
|
|
200–500
|
3625
|
1201
|
33.82 (32.68, 34.97)
|
1.71 (1.08–2.72)
|
50.9
|
0.71
|
< 200
|
2511
|
700
|
21.97 (20.57, 23.36)
|
1.04 (0.79–1.37)
|
77.2
|
0.51
|
Age (36)
|
|
|
|
|
|
|
< 20
|
1064
|
181
|
13.81 (11.86, 15.77)
|
1
|
|
|
20–40
|
6824
|
2393
|
39.59 (38.70, 40.47)
|
1.63 (1.15–2.61)
|
42.3
|
0.06
|
40–60
|
2968
|
1295
|
46.33 (44.93, 47.74)
|
2.49 (1.62–3.82)
|
54.2
|
0.09
|
> 60
|
181
|
75
|
43.78 (37.19, 50.36)
|
2.39 (1.56–3.66)
|
0.0
|
0.48
|
df: degrees of freedom. |
Risk factors for prevalence of latent Toxoplasmosis
With respect to risk factors associated with LT, our results showed that PLWH who consumed raw/undercooked meat (Odds Ratio [OR], 2.01; 95% CI, 1.19–3.9) and those who were in frequent contact with soil (OR, 3.01; 95% CI, 1.5–6.04) were more likely to be seropositive compared with other PLWH (S3 and S4 Figs). Moreover prevalence rates with significantly higher in PLWH who were older in age and had lower CD4 + lymphocyte counts. PLWH in ages 20–40 (OR, 1.63; 95% CI, 1.15–2.61), 40–60 (OR, 2.49; 95% CI, 1.62–3.82) and > 60 (OR, 2.39; 95% CI, 1.56–3.66) (S5-7 Figs) and those with number of CD4 200–500 (OR, 1.71; 95% CI, 1.08–2.72) and lower than 200 (OR, 1.04; 95% CI, 0.79–1.37) were more likely to be seropositive as compared with other PLWH (S8-9 Figs). With respect to other risk factors associated with LT, our results showed that female patients, those who lived in rural areas, those who were cat or dog owners, and those who consumed raw/unwashed vegetables or consumed untreated water were at more, but non-significant greater, risk to acquire infection. More details are given in Table 3 and S10-15 Figs. In Egger’s test we did not identify any significant publication bias (Table 3).
Global prevalence of acute Toxoplasmosis
The global prevalence of AT in PLWH, when data for all 65 datasets representing 32 countries were pooled, was 1.3% (95%CI, 0.9–1.8%; 289/17,705). The heterogeneity between studies was significant (I2 = 79.1%, P < 0.001). With respect to WHO-epidemiological regions, the highest prevalence rates were found in South America (2.0%; 0.1–5.4%), and then the Eastern Mediterranean region (1.8%; 0.7–3.3%), and the lowest prevalence rate was found in the European region (0.6%; 0.2–1.3%). The pooled prevalence rates in other WHO regions were: 1.6% (0.5–3.1%) in North America, 1.3% (0.9–1.8%) in South-East Asia, 1.2% (0.2–2.6%) in the Western Pacific and 0.9% (0.2–1.2%) in Africa (Table 4 and Fig. 1B). Moreover, we estimated that approximately 492,700 (341,100–682,200) PLWH worldwide were affected by AT. Our estimates demonstrated that countries in the African region, has the largest number of PLWH with AT (231,300; 51,400–308,400), accounting for approximately 47% of cases of HIV-AT co-infection worldwide. Additional details pertaining to the prevalence and burden of AT in PLWH in WHO-regions and individual countries are given in Table 4 and Fig. 1B.
Table 4
Global, regional and national pooled prevalence of acute toxoplasmosis (AT) among people living with HIV (PLWH) (results from 65 studies performed in 31 countries).
WHO regions/ country
|
Number datasets
|
Number of PLWH screened (total)
|
Number of PLWH with AT
|
Pooled prevalence (95% CI)
|
Estimated number of PLWH individuals*
|
Estimated number of PLWH with AT
|
Global
|
65
|
17705
|
289
|
1.3 (0.9–1.8)
|
37,900,000
|
492,700 (341,100–682,200)
|
South Americas
|
4
|
863
|
20
|
2.0 (0.1–5.4)
|
1,900,000
|
38,000 (1900–102,600)
|
Brazil
|
4
|
863
|
20
|
2.0 (0.1–5.4)
|
900,000
|
38,000 (1900–102,600)
|
African region
|
15
|
2505
|
32
|
0.9 (0.2–1.2)
|
25,700,000
|
231,300 (51,400–308,400)
|
Ethiopia
|
1
|
150
|
0
|
1.1 (0.2–2.4)
|
690,000
|
7,590 (1,380–16,560)
|
Nigeria
|
1
|
111
|
1
|
0.9 (0.1–4.9)
|
1,900,000
|
17,100 (1900–93,100)
|
Burkina Faso
|
2
|
497
|
0
|
0.1 (0.0–0.4)
|
96,000
|
96 (0-384)
|
Cameroon
|
2
|
223
|
14
|
5.4 (2.7–8.9)
|
540,000
|
29,160 (14,580–48,060)
|
Ghana
|
2
|
519
|
1
|
0.1 (0.0–0.8)
|
330,000
|
330 (0–2,640)
|
South Africa
|
2
|
407
|
7
|
1.4 (0.4–2.9)
|
7,700,000
|
107,800 (30,800–223,300)
|
Zambia
|
1
|
69
|
0
|
0.1 (0.0–5.2)
|
1,200,000
|
1,200 (0–62,400)
|
Canary island (Spain)
|
1
|
157
|
1
|
0.6 (0.0–3.5)
|
140,000
|
840 (0–4900)
|
Botswana
|
1
|
46
|
0
|
0.1 (0.0–7.7)
|
370,000
|
370 (0–28,490)
|
Togo
|
1
|
56
|
2
|
3.6 (0.4–12.3)
|
110,000
|
3,960 (440–13,530)
|
Eastern Mediterranean
|
15
|
2125
|
51
|
1.8 (0.7–3.3)
|
400,000
|
7,200 (2,800–13,200)
|
Iran
|
13
|
1999
|
42
|
1.5 (0.6–2.7)
|
61,000
|
915 (366–1,647)
|
Saudi Arabia
|
1
|
50
|
9
|
18.0 (8.6–31.4)
|
13,000⁂
|
2,340 (1,118–4,082)
|
Bahrain
|
1
|
76
|
0
|
0.1 (0.0–4.7)
|
260⁂
|
2 (0-12.2)
|
European region
|
15
|
6447
|
67
|
0.6 (0.2–1.3)
|
2,500,000
|
15,000 (5,000–32,500)
|
Spain
|
1
|
63
|
6
|
9.5 (3.6–19.6)
|
150,000
|
14,250 (5,400–29,400)
|
Turkey
|
2
|
788
|
0
|
0.1 (0.0–0.2)
|
14,800⁂
|
15 (0–29.6)
|
United Kingdom
|
1
|
500
|
7
|
1.4 (0.6–2.9)
|
101,600
|
1,422 (609–2,946)
|
France
|
2
|
1715
|
14
|
0.3 (0.0–0.7)
|
180,000
|
540 (0–1,260)
|
Romania
|
2
|
224
|
2
|
0.1 (0.0–1.0)
|
18,000
|
18 (0–180)
|
Czech Republic
|
2
|
1302
|
14
|
0.8 (0.3–1.4)
|
4400
|
35 (13–61)
|
Croatia
|
1
|
166
|
2
|
1.2 (0.1–4.3)
|
1600
|
19 (2–69)
|
Germany
|
1
|
183
|
6
|
3.3 (1.2–7.0)
|
87,000
|
2,871 (1,044–6,090)
|
Denmark
|
1
|
503
|
4
|
0.8 (0.2–2.0)
|
6,200
|
49 (12–124)
|
Switzerland
|
1
|
715
|
12
|
1.7 (0.9–2.9)
|
20,000
|
340 (180–580)
|
Serbia
|
1
|
288
|
0
|
0.1 (0.0–1.3)
|
3000
|
3 (0–39)
|
North America and the Caribbean
|
5
|
1729
|
28
|
1.6 (0.5–3.1)
|
1,700,000
|
27,200 (8,500–52,700)
|
USA
|
4
|
1637
|
27
|
1.7 (0.5–3.6)
|
1,100,000
|
18,700 (5,500–39,600)
|
Mexico
|
1
|
92
|
1
|
1.1 (0.1–5.9)
|
230,000
|
2,530 (230–13,570)
|
South-East Asian Region
|
9
|
3605
|
85
|
1.3 (0.9–1.8)
|
3,800,000
|
49,400 (34,200–68,400)
|
India
|
5
|
1730
|
27
|
1.6 (0.4–3.4)
|
2,200,000⁂
|
35,200 (8,800–74,800)
|
Indonesia
|
3
|
737
|
29
|
3.9 (2.5–5.4)
|
640,000
|
24,960 (16,000–34,560)
|
Thailand
|
2
|
1138
|
29
|
1.5 (0.8–2.3)
|
480,000
|
7,200 (3,840–11,040)
|
Western Pacific Region
|
3
|
441
|
6
|
1.2 (0.2–2.6)
|
1,900,000
|
22,800 (3,800–49,400)
|
China
|
1
|
259
|
3
|
1.2 (0.2–3.3)
|
900000⁂
|
10,800 (1,800–29,700)
|
Malaysia
|
2
|
182
|
3
|
1.5 (0.1–4.1)
|
87,000
|
1,305 (87–3,567)
|
Abbreviations: NA: not applicable |
WHO regions are sorted according to prevalence rates |
Countries are sorted according to number of studies included |
Subgroup and meta-regression analyses according to socio-demographic and study characteristics
In subgroup analyses, when the pooled prevalence was stratified according to the income-level of a country, the highest prevalence rates of AT were estimated for countries with lower-middle income-levels (1.8%, 0.7–3.2%) and the lowest for those with low income-levels (0.4%, 0.0–1.9%). Based on HDI level, the highest prevalence rates were seen in countries with low HDI-levels (1.4%, 0.1–1.3%) and the lowest prevalence rates in countries with high HDI-levels (1.3%, 0.7–2.0%) (Table 2). Moreover meta-regression analyses revealed a non-significant decreasing trend in prevalence in countries with increasing per capita income (C = -0.00082; P-value = 0.88) and HDI levels (C = -0.0056; P-value = 0.92) in a country (Fig. 2D and E). Sub-group analysis on year of study showed higher prevalence rates after 2010. This increasing trend was non-significant in meta-regression analysis (C = 0.0002; P-value = 0.7) (Fig. 2F). In subgroup analyses, according to type of study, the highest prevalence rates were estimated in the case-control (2.6%, 0.8–5.0%), and then in prospective cohort (2.6%, 0.8–5.0%) studies, and the lowest prevalence rates were estimated in retrospective cohorts (1.0%, 0.3–2.0%). Subgroup analysis based on diagnostic methods showed that prevalence rates were similar when studies used both IgG-IgM tests (1.2%, 0.7–1.8%) and seroconversion (1.2%, 0.8–1.7%). More subgroup analyses and details are given in Table 2.