Abstract
Giardia duodenalis is one of the major causes of diarrhea among humans, especially in young children. Statistical analysis revealed that the pooled prevalence of G. duodenalis in humans, dogs, and cats was 9.72% (10,921/112383), 15.60% (7510/48140), and 14.53% (1125/7740), respectively. Unquestionably, the canine-specific assemblages C and D and the feline-specific assemblage F were the dominant genotypes in dogs and cats, respectively. Additionally, the prevalence of zoonotic G. duodenalis assemblages (A and B) in dogs and cats was 23.07% (875/3792) and 41.42% (169/408), respectively, implying that the potential transmission of G. duodenalis from dogs and cats to human infection cannot be ignored. The highest frequency of potentially zoonotic assemblages was found among working dogs (3.55%, 25/705) and the 1–5 age group (22.92%, 11/48). In summary, dogs and cats have a significant role in the zoonotic transmission of G. duodenalis due to their close contact with humans and the higher frequency presence of zoonotic assemblages. Further studies are necessary to explore the presence of G. duodenalis among humans and animals and in environmental samples. Researchers should adopt a one-health approach to gain a deeper understanding of G. duodenalis in dogs and cats and potential transmission routes to humans.
Keywords: Giardia duodenalis, Prevalence, Assemblages, Dogs, Cats, Zoonotic potential
Graphical abstract
1. Introduction
Giardia duodenalis, also known as G. intestinalis or G. lamblia, is a globally distributed parasite widely reported in humans and many animals worldwide [1], first discovered in 1681 by Leeuwenhoek [2]. G. duodenalis infection causes watery diarrhea in 280 million people globally [3], including 28.5 million human giardiasis cases in China annually [4,5]. The giardiasis symptoms include watery diarrhea, vomiting, abdominal pain, malabsorption, and other associated symptoms, particularly in young children [6]. For example, G. duodenalis is associated with approximately 15,000 to 17,000 enteritis cases in children in the United States of America each year [7].
G. duodenalis life cycle consists of two stages: rapidly multiplying trophozoites and environmentally hardy cysts [8]. Trophozoites are the vegetative form of G. duodenalis that replicates in the host's small intestine. On the contrary, cysts are the environmentally stable phase of the parasite's life cycle, which are released into the environment in feces and transmitted via the fecal-oral route. Cysts release in the feces contribute to zoonotic transmission of G. duodenalis from one host into the environment and ingestion by another host, ultimately leading to waterborne or foodborne outbreaks [2,[9], [10], [11]]. While several drugs have been approved for treating giardiasis in humans, treatment failure is common, and no vaccine is available [2,[12], [13], [14]].
G. duodenalis is a multispecies complex with eight identified assemblages (A to H), genetically diverse within the species [15]. Among them, assemblages A and B predominantly infect humans and various animals, displaying a high potential for zoonotic transmission [1]. Assemblage A is further divided into AI, AII, and AIII sub-assemblages, and host adaptation has been observed among these three sub-assemblages. For example, sub-assemblage AI predominantly infects animals, sub-assemblage AII infects humans, and sub-assemblage AIII is widely detected in wild ruminants [2,5,16]. The other G. duodenalis assemblages demonstrated host adaptation, with assemblages C and D primarily infecting dogs and cats, assemblage E primarily infecting ungulate animals (cattle, sheep, goats, and pigs), assemblage F mainly infects felines, assemblage G primarily infects rodents and assemblage H is primarily associated with seals [15]. The genotyping methods for G. duodenalis are similar to those for other intestinal protozoa. They typically include the conventional PCR, nested PCR, and quantitative PCR. Among these methods, nested PCR is the most commonly utilized genotyping tool in laboratory settings. Common genotyping loci for Giardia include the SSU rRNA, elongation factor 1 alpha (ef-1), β-giardin (bg), glutamate dehydrogenase (gdh), and triosephosphate isomerase (tpi) genes. However, the SSU rRNA and ef-1 gene loci are the most commonly used for genotyping [2,5,16], including in whole-genome sequencing [17].
Dogs and cats significantly impact our daily lives, providing emotional support and companionship to humans as beloved pets. While G. duodenalis assemblages C and D, and F are primarily associated with dogs and cats, respectively, zoonotic assemblages A and B are also frequently detected in these animals [1]. However, although there are many reports of G. duodenalis infections in dogs and cats, there are few comprehensive assessments of potential zoonotic transmission of G. duodenalis from these animals. Therefore, this review aims to assess the zoonotic potential transmission of G. duodenalis from dogs and cats to humans by analyzing the G. duodenalis prevalence, risk factors, and genotype distributions.
2. Search strategy and selection criteria
We searched PubMed, Web of Science, MEDLINE, ScienceDirect, and the China National Knowledge Infrastructure for all peer-reviewed publications written in English and Chinese documenting the prevalence of G. duodenalis. The search terms used included “Giardia” AND “human”, OR “giardiasis” AND “human” for G. duodenalis populations in humans; “Giardia” AND “dog,” OR “giardiasis” AND “dog” for G. duodenalis populations in dogs; and “Giardia” AND “cat,” OR “giardiasis” AND “cat” for G. duodenalis populations in cats.
All the publications related to the molecular identification of G. duodenalis in humans, dogs, and cats published before December 31, 2022, were screened. First, their titles and abstracts were screened. Subsequently, the full texts were screened for the molecular prevalence records. Finally, the occurrence and genotype distribution of G. duodenalis in humans, dogs, and cats were recorded (Table S1).
3. Molecular epidemiology of G. duodenalis in human
3.1. Molecular prevalence of G. duodenalis
G. duodenalis infections in humans have been molecularly identified in at least 55 countries, with the molecular prevalence ranging from 0.03% (9/26886) in Xinjiang, China [18] to 82.05% (32/39) in Turkey [19]. The pooled molecular prevalence of G. duodenalis in humans is at 9.72% (10,921/112383), with infection rates ranging from 0.40% (210/51924) in China to 62.22% (28/45) in Tanzania. The prevalence of G. duodenalis in humans is highest in Tanzania (62.22%, 28/45), followed by the United Arab Emirates (46.75%, 108/231) and Guinea Bissau (37.06%, 159/429). Conversely, relatively low prevalence rates have been reported in China (0.40%, 210/51924), Romania (0.42%, 33/7805), and Portugal (1.29%, 3/232) (Table 1).
Table 1.
Molecular prevalence and assemblage distributions of Giardia duodenalis in human worldwide.
| Locations | Total No. | Positive No. | Infection rate % | No. genotyped | Assemblage distributions | Sub-assemblage A distributions |
|---|---|---|---|---|---|---|
| Albania | 125 | 22 | 17.60% | 22 | A (10), B (12) | |
| Argentina | 384 | 137 | 35.68% | 84 | A (13), B (69), D (1), mix (1) | AII (4), AIII (7) |
| Australia | 440 | 96 | 21.82% | 66 | A (19), B (47) | AI (1), AII (9) |
| Bangladesh | 2659 | 336 | 12.64% | 305 | A (38), B (250), mix (17) | AI (8), AII (22) |
| Belgium | 373 | 15 | 4.02% | 72 | A (16), B (54), mix (2) | AII (2) |
| Brazil | 6329 | 1122 | 17.73% | 808 | A (468), B (310), C (6), D (1), E (15), F (1), mix (7) | AI (120), AII (202), AIII (34) |
| Canada | 818 | 110 | 13.45% | 110 | A (66), B (40), mix (4) | AI (20), AII (7) |
| China | 51,924 | 210 | 0.40% | 144 | A (80), B (47), C (16), mix (1) | AI (16), AII (27) |
| Colombia | 235 | 31 | 13.19% | 24 | A (20), B (4) | |
| Côte d'Ivoire Ivory Coast | 9 | 2 | 22.22% | |||
| Cuba | 95 | 20 | 21.05% | 20 | A (9), B (11) | |
| Czech Republic | 1 | 1 | B (1) | |||
| Egypt | 2042 | 474 | 23.21% | 381 | A (129), B (179), C (1), E (27), mix (45) | AII (103) |
| Ethiopia | 978 | 246 | 25.15% | 104 | A (37), B (52), mix (15) | AI (1), AII (27) |
| Europe | 1658 | 1658 | A (714), B (930), C (2), D (4), E (4), F (4) | AI (149), AII (466) | ||
| France | 50 | 50 | A (9), B (41) | AII (8) | ||
| Gabon | 241 | 33 | 13.69% | |||
| Germany | 271 | 18 | 6.64% | 17 | A (14), B (3) | AI (5), AII (9) |
| Ghana | 95 | 10 | 10.53% | 5 | A (3), B (2) | |
| Guinea Bissau | 429 | 159 | 37.06% | |||
| India | 1496 | 346 | 23.13% | 336 | A (101), B (183), C (3), D (3), mix (46) | AI (6), AII (2) |
| Iran | 1211 | 394 | 32.54% | 279 | A (200), B (69), mix (10) | AII (160) |
| Italy | 2003 | 160 | 7.99% | 152 | A (81), B (57), mix (14) | AI (8), AII (57) |
| Jamaica | 285 | 19 | 6.67% | 19 | A (19) | AI (3), AII (15) |
| Japan | 26 | 24 | A (14), B (10) | AI (12) | ||
| Kenya | 172 | 30 | 17.44% | 30 | A (4), B (26) | |
| Korea | 7 | 7 | A (7) | |||
| Malaysia | 2027 | 356 | 17.56% | 309 | A (155), B (145), mix (9) | AII (30) |
| Mexico | 395 | 116 | 29.37% | 116 | A (110), mix (6) | AI (72), AII (38) |
| Mongolia | 419 | 14 | 3.34% | |||
| Mozambique | 4847 | 1488 | 30.70% | 227 | A (23), B (199), mix (5) | AI (2), AII (15) |
| Myanmar | 172 | 19 | 11.05% | 19 | A (6), B (13) | |
| Nepal | 6638 | 311 | 4.69% | 35 | A (7), B (26), mix (2) | |
| Netherlands | 892 | 116 | 13.00% | 116 | A (43), B (73) | AI (7), AII (1) |
| New Zealands | 66 | 6 | 9.09% | 5 | A (1), B (4) | |
| Nicaragua | 119 | 119 | A (25), B (94) | AII (16) | ||
| Norway | 84 | 84 | A (3), B (81) | AII (3) | ||
| Peru | 2376 | 539 | 22.69% | 205 | A (80), B (103), mix (22) | AI (9), AII (65) |
| Poland | 232 | 3 | 1.29% | 3 | A (2), B (1) | AII (2) |
| Portugal | 190 | 32 | 16.84% | 32 | A (27), B (5) | AI (25), AII (2) |
| Qatar | 54 | 54 | A (9), B (30), mix (15) | AII (6) | ||
| Romania | 7805 | 33 | 0.42% | 30 | A (27), B (3) | AII (27) |
| Saudi Arabia | 1612 | 97 | 6.02% | 40 | A (23), B (15), mix (2) | AI (12), AII (11) |
| Slovakia | 1262 | 53 | 4.20% | 27 | A (10), B (17) | AI (2), AII (8), BIII (5), BIV (3) |
| South Africa | 968 | 92 | 9.50% | |||
| Spain | 1943 | 634 | 32.63% | 259 | A (79), B (176), mix (4) | AI (44), AII (31), AIII (1), AII/AIII (2) |
| Sweden | 207 | 207 | A (73), B (128), mix (6) | AII (64) | ||
| Tanzania | 45 | 28 | 62.22% | 28 | A (6), B (22) | AII (3) |
| Thailand | 989 | 154 | 15.57% | 133 | A (51), B (46), C (1), F (1), mix (34) | AII (21) |
| Tibet | 1015 | 175 | 17.24% | |||
| Turkey | 4430 | 189 | 4.27% | 100 | A (52), B (46), mix (2) | AI (3), AII (21), AII/AIII (8) |
| Uganda | 1136 | 132 | 11.62% | 89 | A (35), B (46), mix (8) | AI (1), AII (10) |
| United Arab Emirates | 231 | 108 | 46.75% | 82 | A (37), B (37), mix (8) | AI (1), AII (6) |
| United Kingdom | 79 | 28 | 35.44% | 28 | A (26), B (2) | AI (25), AII (1) |
| United States | 2 | 2 | B (2) | |||
| Total | 112,383 | 10,921 | 9.72% | 7067 | A (2981), B (3711), C (29), D (9), E (46), F (6), mix (285) | AI (552), AII (1501), AIII (42), AII/AIII (10), BIII (5), BIV (3) |
In China, G. duodenalis infections in humans have been recorded in at least eight provinces, municipalities, or autonomous regions (Table S2), with a pooled molecular prevalence of 0.40% (210/51924). However, the prevalence varies across the different regions, ranging from 0.03% (9/26886) in Xinjiang [18] to 9.46% (7/74) in Shanghai [20]. Furthermore, analysis of Giardia occurrence in humans in China revealed the highest prevalence rates in Heilongjiang (10.17%, 42/413), followed by Anhui (4.12%, 40/972) and Shanghai (3.39%, 28/825). Conversely, relatively low prevalence rates were reported in Xinjiang (0.03%, 9/26886) and Jilin (0.04%, 3/8396) (Table S2).
3.2. Genotype distributions
Of the 10,921 positive samples for G. duodenalis in humans, 7067 were successfully genotyped using SSU rRNA, bg, gdh, tpi, or multiple loci (Table 1). Statistical analysis revealed that the human-specific assemblages A and B were responsible for 42.18% (2981/7067) and 52.51% (3711/7067) of the genotyped samples, respectively. On the contrary, relatively low samples were infected with the felid-specific assemblage F (0.09%, 6/7067).
Of the 2105 human G. duodenalis assemblage A isolates identified, 26.34% (552/2095), 71.65% (1501/2095), and 2.00% (42/2095) were classified in sub-assemblages AI, AII and AIII, respectively. These results are consistent with previous studies [5], which revealed that sub-assemblage AI is predominantly found in animals and sub-assemblage AII in humans.
In China, out of the 210 positive samples for G. duodenalis in humans, only 114 samples were successfully genotyped using SSU rRNA, bg, gdh, tpi, or multiple loci (Table 1). Statistical analysis revealed that the human-specific assemblages A and B were responsible for 55.56% (80/144) and 32.64% (47/144)genotyped samples, respectively, followed by the canine-specific assemblage C (11.11%, 16/144). Additionally, one isolate exhibited a mixed assemblage (A/B).
The data revealed that assemblages A and B are the major G. duodenalis genotypes infecting humans, consistent with previous studies [1]. Besides, humans can also be infected by canine-specific assemblages C and D and felid-specific assemblage F (including 38 assemblages C or D and 6 assemblages F).
4. Molecular epidemiology of G. duodenalis in dogs
4.1. Molecular prevalence of G. duodenalis
G. duodenalis infections in dogs have been documented in at least 38 countries, with the molecular prevalence ranging from 1.17% (8/682) in Qinghai, China [21], to 75.75% (25/33) in Italy [22]. The pooled molecular prevalence is at 15.60% (7510/48140), with infection rates ranging from 2.86% (2/70) in Singapore to 51.22% (63/123) in the Czech Republic. The highest G. duodenalis prevalence in dogs was reported in the Czech Republic (51.22%, 63/123), Argentina (44.44%, 16/36), and the Netherlands (31.38%, 107/341). Conversely, relatively low prevalence rates have been reported in Singapore (2.86%, 2/70), Iran (4.04%, 42/1040), and Ecuador (4.82%, 4/83) (Fig. 1).
Fig. 1.
Molecular prevalence and assemblages distributions of Giardia duodenalis in dogs (A) and cats (B) in worldwide and China.
In China, G. duodenalis infections in dogs have been recorded in at least 13 provinces, municipalities, or autonomous regions (Table S3), with a pooled molecular prevalence of 11.49% (1156/10062). The prevalence of G. duodenalis infections in dogs varied across the different regions, ranging from 1.17% (8/682) in Qinghai [21] to 63.50% (54/85) in Jilin [23]. The highest prevalence was reported in Shanghai (26.29%, 260/989), Yunnan (13.74%, 36/262), and Beijing (12.75%, 62/485). Conversely, a relatively low prevalence of G. duodenalis infections in dogs was reported in Qinghai (2.54%, 8/710), Fujian (3.17%, 10/315), and Xinjiang (3.64%, 22/604) (Fig. 1).
4.2. Risk factors for G. duodenalis infection in dogs
Several factors contribute to the variation in G. duodenalis infection rates in dogs (Table 3). For example, dogs in shelters exhibited the highest prevalence rate (28.02%, 1383/4936), followed by working dogs (15.18%, 107/705), stray dogs (15.24%, 199/1306), and pet dogs had the lowest infection rate (13.97%, 983/7039). In this study, working dogs encompassed shepherds, police, and hunting dogs. Interestingly, among the pet dogs, those in pet markets had a much higher infection rate (20.24%, 265/1309) compared to those in pet hospitals (14.16%, 142/1003), kennels (13.11%, 83/633), and families (12.04%, 493/4094). This difference may be attributed to the varying hygiene conditions, the level of care provided by breeders, and the immune status of the animals.
Table 3.
Giardia duodenalis infections in dogs under different factors.
| Factors | Positive No. | Total No. | Infection rate % | P-vlaue | χ2 (95%CI) | Assemblage distributions | Sub-assemblage distribution | ||
|---|---|---|---|---|---|---|---|---|---|
| Source | |||||||||
| Pet | Pet family | 493 | 4094 | 12.04% | Reference | Reference | A (15), C (21), D (21), F (1), mix (7) | ||
| Pet hospital | 142 | 1003 | 14.16% | 0.069 | 3.306 (0.679–1.015) | A (6), C (15), D (45), mix (15) | |||
| Pet kennels | 83 | 633 | 13.11% | 0.444 | 0.587 (0.707–1.164) | C (7), D (7), mix (1) | |||
| Pet market | 265 | 1309 | 20.24% | 0.000 | 55.329 (0.458–0.636) | A (27), B (2), C (64), D (104), E (1), mix (16) | |||
| Subtotal | 983 | 7039 | 13.97% | 0.004 | 8.324 (0.751–0.947) | A (51), B (2), C (107), D (175), E (1), F (1), mix (35) | |||
| Working dogs | 107 | 705 | 15.18% | 0.020 | 5.404 (0.610–0.959) | A (25), C (2), D (2) | AI (25) | ||
| Shelter dogs | 1383 | 4936 | 28.02% | 0.000 | 347.056 (0.314–0.394) | A (2), B (1), C (91), D (85), mix (23) | AI (1), AII (1) | ||
| Stray dogs | 199 | 1306 | 15.24% | 0.003 | 9.049 (0.637–0.910) | A (9) | AI (9) | ||
| Age | |||||||||
| ≤1y | 0-3 m | 173 | 727 | 23.80% | Reference | Reference | C (3), D (3) | ||
| 3-6 m | 443 | 3462 | 12.80% | 0.000 | 57.966 (1.746–2.593) | A (4), C (24), D (70), F (1), mix (11) | AI (2) | ||
| 6-12 m | 662 | 3704 | 17.87% | 0.000 | 13.945 (1.186–1.734) | A (22), C (30), D (32), mix (8) | AI (4) | ||
| Subtotal | 1278 | 7893 | 16.19% | 0.000 | 27.858 (1.353–1.943) | A (29), C (57), D (105), mix (19) | AI (6) | ||
| >1y | 932 | 11,210 | 8.31% | 0.000 | 194.824 (2.867–4.137) | A (11), C (23), D (28), mix (1) | AI (3) | ||
| 1-5y | 761 | 7888 | 9.65% | 0.000 | 137.859 (2.427–3.524) | A (11), C (14), D (22), mix (1) | AI (3) | ||
| >5y | 171 | 3322 | 5.15% | 0.000 | 266.835 (4.573–7.241) | C (9), D (6) | |||
| Gender | |||||||||
| Female | 847 | 4972 | 17.04% | Reference | Reference | A (20), C (28), D (39), mix (3) | AI (5) | ||
| Male | 888 | 5681 | 15.63% | 0.050 | 3.835 (1.000–1.228) | A (15), C (47), D (43), F (1), mix (7) | AI (4) | ||
| Feeding methods | |||||||||
| Captivity | 23 | 210 | 10.95% | Reference | Reference | ||||
| Free-range | 41 | 245 | 16.73% | 0.077 | 3.128 (0.354–1.058) | ||||
| Sterilization | |||||||||
| Yes | 61 | 333 | 18.32% | Reference | Reference | ||||
| No | 195 | 834 | 23.38% | 0.059 | 3.562 (0.533–1.013) | ||||
| Diarrhea status | |||||||||
| Yes | 541 | 2356 | 22.96% | Reference | Reference | B (1), C (28), D (61), mix (16) | |||
| No | 585 | 3377 | 17.32% | 0.000 | 27.966 (1.248–1.622) | A (1), B (1), C (27), D (88), mix (22) | AI (1) | ||
| Living environment | |||||||||
| Urban | 16 | 663 | 2.41% | Reference | Reference | ||||
| Rural | 31 | 263 | 11.79% | 0.000 | 34.324 (0.099–0.345) | ||||
| Breed | |||||||||
| purebred dog | 28 | 120 | 23.33% | Reference | Reference | ||||
| hybrid dogs | 66 | 162 | 40.74% | 0.002 | 9.400 (0.261–0.749) | ||||
| Deworming | |||||||||
| Yes | 55 | 1058 | 5.20% | Reference | Reference | C (1), D (4) | |||
| No | 64 | 560 | 11.43% | 0.000 | 20.859 (0.292–0.619) | C (4), D (10), F (1) | |||
| Season | |||||||||
| Spring | 120 | 523 | 22.94% | Reference | Reference | C (9), D (11) | |||
| Summer | 92 | 373 | 24.66% | 0.550 | 0.357 (0.666–1.242) | C (17), D (22) | |||
| Autumn | 47 | 282 | 16.67% | 0.036 | 4.392 (1.025–2.163) | ||||
| Winter | 89 | 422 | 21.09% | 0.495 | 0.466 (0.817–1.519) | D (2) | , | ||
Furthermore, the prevalence of G. duodenalis in puppies less than one year old (16.19%, 1278/7893) was notably higher compared to other age groups. Interestingly, in the less than one year age group, the prevalence in the 0–3 month age range (23.80%, 173/727) was significantly higher than in the other age groups (Table 3).
However, there was no significant difference in the prevalence of G. duodenalis between female (17.04%, 847/4972) and male (15.63%, 888/5681) dogs (P > 0.05). Similarly, there was no significant difference in the prevalence of G. duodenalis between free-range dogs (16.73%, 41/245) and dogs kept in captivity (10.95%, 23/210) (P > 0.05). Additionally, the difference in prevalence based on the sterilization status of the dogs was insignificant (P > 0.05) (Table 3).
Regarding the diarrhea status, dogs that exhibited diarrhea symptoms had a significantly higher prevalence of G. duodenalis (22.96%, 541/2356) than those without diarrhea symptoms (17.32%, 585/3377) (P < 0.01). Additionally, the prevalence of G. duodenalis in rural dogs (11.79%, 31/263) was significantly higher than in urban dogs (2.41%, 16/663) (P < 0.01). Furthermore, a significantly higher G. duodenalis prevalence was recorded in hybrid dogs than in purebred dogs. Dogs that had not been dewormed in the past month also recorded a significantly higher prevalence of G. duodenalis infections (P < 0.01) (Table 3).
Among the different seasons, the infection rate of G. duodenalis was the highest during summer, with a prevalence of 24.7% (92/373), followed by spring (22.94%, 120/523), winter (21.09%, 89/422), and autumn (16.67%, 47/282) (Table 3).
4.3. Genotype distributions
Among the positive samples for G. duodenalis identified in dogs worldwide, 3792 samples were successfully genotyped using SSU rRNA, bg, gdh, tpi, or multi loci (Table 2), of which 66.59% (2525/3792) were canine-specific assemblages C and D. Specifically, 32.49% (1232/3792) of the successfully genotyped samples belonged to assemblage C and 34.10% (1293/3792) to assemblage D. Zoonotic assemblages A and B accounted for 23.07% (875/3792) of the positive samples, with assemblage A accounting for 16.85% (639/3792) and assemblage B for 6.22% (236/3792). There was a relatively low prevalence of the ruminant-specific assemblage E, which accounted for only 0.37% (14/3792) of the samples, and the felid-specific assemblage F (0.11%, 4/3792). Additionally, there was a considerable number (9.86%, 374/3792) of mixed infections, including assemblages C/D (63.37%, 237/374), A/B (14.17%, 53/374), and A/C (7.75%, 29/374) (Supplementary Fig. S1).
Table 2.
Molecular prevalence and assemblage distributions of Giardia duodenalis in dogs worldwide.
| Locations | Total No. | Positive No. | Infection rate % | No. genotyped | Assemblage distributions | Sub-assemblage A distributions |
|---|---|---|---|---|---|---|
| Argentina | 36 | 16 | 44.44% | 16 | A (13), C (3) | |
| Australia | 2601 | 286 | 11.00% | 62 | C (29), D (30), E (1), mix (2) | |
| Brazil | 1744 | 498 | 28.56% | 179 | A (87), B (13), C (36), D (38), mix (5) | AI (50), AII (23) |
| Cambodia | 94 | 10 | 10.64% | 10 | B (2), C (4), mix (4) | |
| Canada | 3406 | 388 | 11.38% | 108 | B (3), C (37), D (67), E (1) | |
| China | 10,062 | 1156 | 11.49% | 797 | A (195), B (8), C (260), D (287), E (5), F (3), mix (39) | AI (51) |
| Columbia | 4 | 4 | C (2), D (2) | |||
| Croatia | 96 | 96 | 93 | A (4), B (10), C (18), D (21), mix (40) | ||
| Cuba | 98 | 11 | 11.22% | 9 | A (5), B (4) | AI (4), AII (1) |
| Czech Republic | 123 | 63 | 51.22% | 54 | C (21), D (32), mix (1) | |
| Ecuador | 83 | 4 | 4.82% | 0 | ||
| Egypt | 108 | 19 | 17.59% | 0 | ||
| Germany | 1393 | 232 | 16.69% | 184 | A (46), B (3), C (38), D (51), F (1), mix (45) | |
| Greece | 879 | 222 | 25.26% | 99 | A (5), C (45), D (28), mix (21) | AI (4), AII (1) |
| India | 202 | 40 | 19.80% | 17 | A (8), B (3), mix (6) | AI (1), AII (4) |
| Iran | 1040 | 42 | 4.04% | 32 | A (5), B (6), C (13), D (6), mix (2) | AII (1) |
| Israel | 854 | 121 | 14.16% | 0 | ||
| Italy | 6744 | 1318 | 19.54% | 558 | A (64), B (8), C (248), D (207), mix (31) | AI (17) |
| Jamaica | 225 | 44 | 19.56% | 44 | A (44) | AI (13), AII (31) |
| Japan | 28 | 28 | 28 | A (14), C (1), D (10), mix (3) | ||
| Korea | 842 | 166 | 19.71% | 61 | C (26), D (35) | |
| Malaysia | 132 | 12 | 9.09% | 11 | B (2), C (8), D (1) | |
| Mexico | 825 | 185 | 22.42% | 48 | A (48) | AI (30), AII (13) |
| Netherlands | 341 | 107 | 31.38% | 103 | A (3), C (27), D (55), mix (18) | AI (2) |
| Nicaragua | 58 | 13 | 22.41% | 13 | A (2), B (5), C (3), D (3) | |
| Peru | 604 | 88 | 14.57% | 67 | C (9), D (32), mix (26) | |
| Philippines | 165 | 19 | 11.52% | 19 | C (17), D (2) | |
| Poland | 770 | 94 | 12.21% | 58 | A (7), B (1), C (23), D (25), E (1), mix (1), | |
| Portugal | 206 | 55 | 26.70% | 43 | B (1), C (19), D (23), | |
| Romania | 124 | 26 | 20.97% | 0 | ||
| Singapore | 70 | 2 | 2.86% | 2 | C (2) | |
| Spain | 1370 | 380 | 27.74% | 170 | A (33), B (62), C (22), D (40), E (6), mix (7) | AII (11), AIII (1) |
| Switzerland | 1 | 1 | 1 | C (1) | ||
| Thailand | 1054 | 134 | 12.72% | 56 | A (2), C (16), D (36), mix (2) | |
| Turkey | 473 | 89 | 18.82% | 89 | B (51), mix (38) | |
| United Kingdom | 878 | 184 | 20.96% | 41 | A (1), C (10), D (29), mix (1) | AI (1) |
| United States | 10,086 | 1329 | 13.18% | 691 | A (53), B (54), C (277), D (228), mix (79) | |
| Vietnam | 354 | 28 | 7.91% | 25 | C (17), D (5), mix (3) | |
| Total | 48,140 | 7510 | 15.60% | 3792 | A (639), B (236), C (1232), D (1293), E (14), F (4), mix (374) | AI (173), AII (85), AIII (1) |
Supplementary Fig. S1.
Distribution of Giardia duodenalis for assemblages (A) and mixed assemblages (B) in the world and China from dogs (left two columns) and cats (right two column)
In this study, 259 canine G. duodenalis assemblage A isolates were identified, belonging to the three sub-assemblages: AI (66.80%, 173/259), AII (32.82%, 85/259), and AIII (0.39%, 1/259). Previous studies revealed that sub-assemblage AI is predominantly found in animals, while sub-assemblage AII is mainly found in humans [5]. This suggests that dogs infected with G. duodenalis may harbor the same genotype as humans, indicating the potential for zoonotic transmission.
In China, 797 positive samples for G. duodenalis in dogs were genotyped using SSU rRNA, bg, gdh, tpi, or multiple loci (Table S3). Among them, the canine-specific assemblages C and D accounted for 68.63% (547/797) of the identified G. duodenalis-positive samples in dogs. Independently, assemblage C accounted for 32.62% (260/797) of the positive samples, and assemblage D for 36.01% (287/797). Zoonotic assemblages A and B were responsible for 25.47% (203/797) of the samples, with assemblage A accounting for 24.47% (195/797) and assemblage B for 1.00% (8/797). The ruminant-specific assemblage E was identified in 0.63% (5/797) of the samples, and the feline-specific assemblage F in 0.38% (3/797). Additionally, there were mixed infections, which accounted for 4.89% (39/797) of the samples, including assemblages C/D (69.23%, 27/39), A/D (20.51%, 8/39) and A/C (10.26%, 4/39). Interestingly, only sub-assemblage AI was identified in dogs in Guangdong and Liaoning provinces in China [24].
5. Molecular epidemiology of G. duodenalis in cats
5.1. Molecular prevalence of G. duodenalis
G. duodenalis infection in cats has been reported in 23 countries worldwide, with an overall pooled prevalence of 14.53% (1125/7740) (Table 4). The prevalence varies across regions, ranging from 1.18% (4/340) in Iran [25] to 40.83% (89/218) in the United States of America [26]. Germany has the highest prevalence of G. duodenalis in cats (73.26%, 63/86), followed by the United States of America (40.83%, 89/218), Australia (21.07%, 208/987), United Kingdom (20.59%, 224/1088), Greece (20.45%, 54/264), Canada (19.23%, 45/234), Turkey (18.81%, 38/202), and the Czech Republic (18.38%, 25/136) (Fig. 1). Generally, most countries have a G. duodenalis infection rate exceeding 15.00%. The United Kingdom (20.59%, 224/1088), Italy (11.03%, 87/789), and China (4.94%, 78/1579) have conducted more epidemiological surveys on G. duodenalis infection in cats, providing additional data on the prevalence of G. duodenalis infection in these countries.
Table 4.
Prevalence and assemblage distributions of Giardia duodenalis in cats worldwide.
| Locations | Total No. | Positive No. | Infection rate % | No. genotyped | Assemblage distributions | Sub-assemblage distribution |
|---|---|---|---|---|---|---|
| Australia | 987 | 208 | 21.07% | 22 | A (9), D (12), F (1) | |
| Brazil | 56 | 56 | 20 | A (9), F (11) | AI (9) | |
| Canada | 234 | 45 | 19.23% | 13 | B (12), C (1) | |
| China | 1579 | 78 | 4.94% | 56 | A (20), B (6), C (3), D (1), F (25), mix (1) | AI (6) |
| Czech Republic | 136 | 25 | 18.38% | 25 | A (2), F (23) | AI (2) |
| Denmark | 284 | 34 | 11.97% | 10 | A (9), F (1) | |
| Egypt | 104 | 5 | 4.81% | |||
| Germany | 86 | 63 | 73.26% | 52 | A (14), B (2), C (1), D (3), F (16), mix (16) | |
| Greece | 264 | 54 | 20.45% | 13 | A (7), F (6) | |
| Iran | 340 | 4 | 1.18% | 4 | A (1), F (3) | AI (1) |
| Italy | 789 | 87 | 11.03% | 69 | A (52), C (2), D (3), F (10), mix (2) | |
| Japan | 345 | 44 | 12.75% | 44 | A (5), C (1), F (31), mix (7) | |
| Korea | 158 | 6 | 3.80% | |||
| Netherlands | 60 | 3 | 5.00% | 2 | A (1), F (1) | |
| Poland | 301 | 17 | 5.65% | 14 | A (3), B (2), D (2), F (7) | |
| Portugal | 22 | 2 | 9.09% | 2 | A (2) | |
| Slovakia | 73 | 6 | 8.22% | 6 | F (6) | |
| Spain | 243 | 14 | 5.76% | 5 | A (1), F (3), mix (1) | |
| Switzerland | 105 | 14 | 13.33% | |||
| Thailand | 66 | 9 | 13.64% | 2 | A (1), D (1) | AI (1) |
| Turkey | 202 | 38 | 18.81% | 8 | B (8) | |
| United Kingdom | 1088 | 224 | 20.59% | |||
| United States | 218 | 89 | 40.83% | 41 | A (3), D (2), F (31), mix (5) | |
| Total | 7740 | 1125 | 14.53% | 408 | A (139), B (30), C (8), D (24), F (175), mix (32) | AI (19) |
In China, G. duodenalis infection in cats has been reported in seven provinces/municipalities (Table S3). The infection rates range from 1.17% (2/171) in Yunnan [27] to 13.45% (23/171) in Shanghai [28]. Thus, Shanghai has the highest prevalence of G. duodenalis infection in cats compared to other regions (Table S4).
5.2. Risk factors for Giardia duodenalis infections in cats
Various factors contribute to the differences in G. duodenalis infection rates in cats (Table 5). For example, stray cats have the highest prevalence (18.27%, 99/542) (P < 0.01), followed by shelter cats (13.48%, 93/690). Pet cats had the lowest infection rate (12.47%, 119/954). Interestingly, among pet cats, there was no significant difference in G. duodenalis infections between cats in pet families, pet hospitals, and pet markets (P > 0.05). However, the G. duodenalis prevalence in cats was slightly higher in kittens less than a year old (8.75%, 47/537) compared to those over a year old (6.71%, 54/805), though the difference was insignificant (P > 0.05). In addition, there were no significant differences in G. duodenalis infections among cats based on gender, feeding methods, living environments, sterilization status, or deworming status (P > 0.05) (Table 5). However, cats with diarrhea had significantly higher G. duodenalis infections (20.05%, 243/1212) than those without diarrhea symptoms (5.35%, 34/635) (P < 0.01).
Table 5.
Giardia duodenalis infection in cats under different factors.
| Factors | Positive no. | Total no. | Infection rate % | P value | χ2 (95%CI) | Assemblage distributions | ||
|---|---|---|---|---|---|---|---|---|
| Source | ||||||||
| Pet | Pet family | 65 | 529 | 12.29% | Reference | Reference | F (2) | |
| Pet hospital | 38 | 303 | 12.54% | 0.915 | 0.011 (0.637–1.498) | |||
| Pet market | 103 | 832 | 12.38% | 0.960 | 0.003 (0.712–1.381) | A (1), B (2), C (2), D (1), F (5) | ||
| Subtotal | 119 | 954 | 12.47% | 0.917 | 0.011 (0.712–1.358) | A (1), B (2), C (2), D (1), F (7) | ||
| Shelter cats | 93 | 690 | 13.48% | 0.540 | 0.376 (0.641–1.263) | A (3), B (4), F (2) | ||
| Stray cats | 99 | 542 | 18.27% | 0.007 | 7.378 (0.447–0.880) | F (10) | ||
| Age | ||||||||
| ≤1y | 47 | 537 | 8.75% | Reference | Reference | A (4), B (2), C (2), D (1), F (3), mix (1) | ||
| >1y | 54 | 805 | 6.71% | 0.164 | 1.934 (0.888–2.004) | A (1), B (4), F (3), mix (2) | ||
| Gender | ||||||||
| Female | 53 | 706 | 7.51% | Reference | Reference | A (2), mix (2) | ||
| Male | 43 | 578 | 7.44% | 0.963 | 0.002 (0.665–1.534) | A (1), mix (1) | ||
| Feeding methods | ||||||||
| Captivity | 9 | 38 | 23.68% | Reference | Reference | |||
| Free-range | 10 | 29 | 34.48% | 0.331 | 0.944 (0.202–1.720) | |||
| Diarrhea status | ||||||||
| Yes | 243 | 1212 | 20.05% | Reference | Reference | |||
| No | 34 | 635 | 5.35% | 0.000 | 70.585 (3.053–6.437) | |||
| Living environment | ||||||||
| Urban | 13 | Reference | Reference | |||||
| Rural | 5 | 48 | 10.42% | 0.225 | 1.475 (1.014–1.229) | |||
| Sterilization | ||||||||
| Yes | 1 | 34 | 2.94% | Reference | Reference | |||
| No | 2 | 78 | 2.56% | 0.910 | 0.013 (0.101–13.145) | |||
| Breed | ||||||||
| Purebred | 20 | 187 | 10.70% | |||||
| Hybrid | ||||||||
| Deworming | ||||||||
| Yes | 1 | 15 | 6.67% | Reference | Reference | |||
| No | 5 | 19 | 26.32% | 0.136 | 2.227 (0.021–1.938) | |||
5.3. Genotype distributions
Of the 1125 positive G. duodenalis samples identified in cats, 408 were successfully genotyped using SSU rRNA, bg, gdh, tpi, or multiple loci (Table 4). Statistical analysis revealed that the felid-specific assemblage F accounted for 42.89% (175/408) of the genotyped samples. Zoonotic assemblages A and B accounted for 34.07% (139/408) and 7.35% (30/408) samples, respectively. However, the canine-specific assemblages C and D accounted for the least number of genotyped samples, with assemblage C accounting for 1.96% (8/408) and assemblage D 5.88% (24/408). Among the G. duodenalis-infected samples, 32 isolates exhibited mixed genotypes, with A/F (56.25%, 18/32) as the predominant mixed genotype, followed by B/F (12.5%, 4/32), and some mixed genotypes (Supplementary Fig. S1).
In China, out of the 78 G. duodenalis positive samples identified in cats, only 56 samples were successfully genotyped using SSU rRNA, bg, gdh, tpi, or multiple loci (Table S3). Of the 56 samples, the felid-specific assemblage F accounted for 44.64% (25/56) of the genotyped samples, followed by zoonotic assemblages A (35.71%, 20/56) and B (10.71%, 6/56). Further analysis revealed only AI G. duodenalis assemblage A subtype was identified in cats. The canine-specific assemblages C and D were the least, with assemblage C accounting for 5.36% (3/56) and assemblage D for 1.79% (1/56). Additionally, one isolate exhibited a mixed assemblage (A/C).
Overall, assemblage F was the major G. duodenalis genotype infecting the cats, consistent with previous studies [1,5].
6. Assessment of potential zoonotic transmission
6.1. Waterborne or foodborne zoonotic transmission
Giardiasis is a significant global health concern and one of the most common causes of waterborne and foodborne diseases worldwide. It accounts for over 280 million human diarrhea cases annually [3]. Besides, several major G. duodenalis outbreaks have been reported globally, highlighting its impact on public health. For example, in 1955, >50,000 people were infected with G. duodenalis through contaminated water in the United States of America [10]. In 2004, another extensive outbreak occurred in Bergen, Norway, affecting over 1500 individuals. This outbreak was traced back to drinking Giardia cysts-contaminated water due to leakage from a septic tank [29]. Since then, >300 outbreaks of giardiasis have been reported worldwide, with exposure to contaminated drinking or recreational water being the primary transmission route [30].
In addition to waterborne transmission, there are also documented cases of foodborne G. duodenalis outbreaks worldwide [10]. For example, G. duodenalis has been detected in fruits and vegetables in various countries, including Bangladesh, Brazil, Costa Rica, Egypt, Ethiopia, Ghana, India, Iran, Italy, Jordan, Norway, Saudi Arabia, Spain, and Sudan [[31], [32], [33], [34], [35], [36], [37], [38], [39]]. The average prevalence of G. duodenalis in these foods has been reported to be 4.8% [40].
These reports highlight the importance of addressing water and food safety measures to prevent G. duodenalis transmission and reduce the occurrence of giardiasis outbreaks.
6.2. Zoonotic potential of G. duodenalis in dogs and cats
G. duodenalis is commonly detected in domestic and wild animals, with a notable presence of zoonotic assemblages A and B. Notably, domestic animals such as sheep, goats, pigs, and calves, and wild animals including bison, wild raccoons, and wild canines harbor G. duodenalis [11,[41], [42], [43], [44], [45], [46], [47], [48]]. Besides, a case-control study revealed that giardiasis was associated with contact with farm animals and pets, particularly pigs, dogs, and cats [49].
An assessment of the zoonotic potential of G. duodenalis in the different breeds of dogs revealed that the highest proportion of zoonotic potential assemblages is in working dogs (86.21%, 25/29). However, the G. duodenalis prevalence is lowest in working dogs (15.18%, 107/705) and highest in shelter dogs (28.02%, 1383/4936) (Table 3), implying that shelter dogs have a higher overall prevalence, but working dogs have a higher zoonotic potential for transmitting the infection.
Moreover, the prevalence of G. duodenalis in dogs decreases with increasing dog age (from 5.15% to 16.19%). However, the zoonotic potential increases with age (13.81% to 22.92%). Interestingly, no potential zoonotic assemblages were identified in dogs older than 5 years (Table 5), though the highest zoonotic potential was in the >5-year age group. Nonetheless, the dog gender and diarrhea status do not significantly influence their zoonotic potential. For cats, it is worth noting that the statistical results regarding zoonotic potential and age groups, particularly in shelter cats and cats over 1 year old, need to be verified with more samples, given the limited sample size (<20 cats) analyzed in this study (Table 6). Thus, further studies with a larger sample size are necessary to confirm these findings and provide more robust insights into the zoonotic potential of G. duodenalis in cats.
Table 6.
Assemblage distributions of Giardia duodenalis in dogs and cats under different factors.
| Animals | Factors | Positive no. | Total no. | Infection rate % | No. of genotyped | Assemblage distribution | Zoonotic potential (no.) |
|---|---|---|---|---|---|---|---|
| Dogs | Source | ||||||
| Pet | 983 | 7039 | 13.97% | 372 | A (51), B (2), C (107), D (175), E (1), F (1), mix (35) | 14.24% (53) | |
| Working dogs | 107 | 705 | 15.18% | 29 | A (25), C (2), D (2) | 86.21% (25) | |
| Shelter | 1383 | 4936 | 28.02% | 203 | A (3), B (1), C (91), D (85), mix (23) | 1.97% (4) | |
| Stray dogs | 199 | 1306 | 15.24% | 9 | A (9) | 100% (9) | |
| Age | |||||||
| ≤1y | 1278 | 7893 | 16.19% | 210 | A (29), C (57), D (105), mix (19) | 13.81% (29) | |
| >1y | 932 | 11,210 | 8.31% | 63 | A (11), C (23), D (28), mix (1) | 17.46% (11) | |
| 1-5y | 761 | 7888 | 9.65% | 48 | A (11), C (14), D (22), mix (1) | 22.92% (11) | |
| >5y | 171 | 3322 | 5.15% | 15 | C (9), D (6) | 0 (0) | |
| Gender | |||||||
| Female | 847 | 4972 | 17.04% | 90 | A (20), C (28), D (39), mix (3) | 22.22% (20) | |
| Male | 888 | 5681 | 15.63% | 113 | A (15), C (47), D (43), F (1), mix (7) | 13.27% (15) | |
| Diarrhea status | |||||||
| Yes | 541 | 2356 | 22.96% | 106 | B (1), C (28), D (61), mix (16) | 0.94% (1) | |
| No | 585 | 3377 | 17.32% | 139 | A (1), B (1), C (27), D (88), mix (22) | 1.44% (2) | |
| Cats | Source | ||||||
| Pet | 119 | 954 | 12.47% | 13 | A (1), B (2), C (2), D (1), F (7) | 23.08% (3) | |
| Shelter | 93 | 690 | 13.48% | 9 | A (3), B (4), F (2) | 77.78% (7) | |
| Stray cats | 99 | 542 | 18.27% | 10 | F (10) | 0 (0) | |
| Age | |||||||
| ≤1y | 47 | 537 | 8.75% | 13 | A (4), B (2), C (2), D (1), F (3), mix (1) | 46.15% (6) | |
| >1y | 54 | 805 | 6.71% | 10 | A (1), B (4), F (3), mix (2) | 50.0% (5) | |
| Gender | |||||||
| Female | 53 | 706 | 7.51% | 4 | A (2), mix (2) | 50.0% (2) | |
| Male | 43 | 578 | 7.44% | 2 | A (1), mix (1) | 50.0% (1) |
Given dogs and cats are common companion animals for humans, they have a higher chance of contact with humans, water, and food. Therefore, further studies are necessary to investigate G. duodenalis in human populations, livestock, pet animals, and environmental samples. It is crucial to adopt a multidisciplinary one-health approach involving zoologists, ecologists, veterinarians, and public health experts to gain a comprehensive understanding of G. duodenalis infections in dogs and cats and potential transmission routes. This collaborative effort will contribute to effective prevention and control strategies for G. duodenalis infections and mitigate the risk of zoonotic transmission.
7. Conclusion
G. duodenalis is an important zoonotic parasite transmitted between dogs, cats, and humans. The worldwide prevalence of G. duodenalis is significant in humans (9.72%), dogs (15.60%), and cats (14.53%). Human-specific assemblages A and B, canine-specific assemblages C and D, and felid-specific assemblages F are the dominant genotypes identified in humans, dogs, and cats, respectively. The zoonotic assemblages A and B cannot be ignored in dogs and cats, as they account for a considerable proportion of dogs and cats infections, respectively.
The following are the supplementary data related to this article.
Raw statistical data on Giardia duodenalis infection in humans,dogs and cats.
Table S2. Molecular prevalence and assemblage distributions of Giardia duodenalis in human in China.
Table S3. Molecular prevalence and assemblage distributions of Giardia duodenalis in dogs in China.
Table S4. Molecular prevalence and assemblage distributions of Giardia duodenalis in cats in China.
Funding
This work was partially supported by the National Natural Science Foundation of China (32102698), the Outstanding Talents of Henan Agricultural University (30501055), and the Henan Postdoctoral Scientific Research Initiation Project (282851).
Declaration of Competing Interest
The authors declare that they have no competing interests.
Contributor Information
Longxian Zhang, Email: zhanglx8999@henau.edu.cn.
Junqiang Li, Email: lijunqiangcool@126.com.
Data availability
Data will be made available on request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Raw statistical data on Giardia duodenalis infection in humans,dogs and cats.
Table S2. Molecular prevalence and assemblage distributions of Giardia duodenalis in human in China.
Table S3. Molecular prevalence and assemblage distributions of Giardia duodenalis in dogs in China.
Table S4. Molecular prevalence and assemblage distributions of Giardia duodenalis in cats in China.
Data Availability Statement
Data will be made available on request.