- Email: [email protected]
Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats
PARINT-01371; No of Pages 3 Parasitology International xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Parasitology International journal homepage: www.elsevier.com/locate/parint
5
F
Moizur Rahman a, Md. Alauddin a, K.M. Mozaffor Hossain a, Md. Hemayetul Islam a, Katsuya Kitoh b, Kisaburo Nagamune c, Yasuhiro Takashima b,⁎
O
4Q3
6 7 8Q4
a
9
a r t i c l e
10 11 12 13 14
Article history: Received 17 February 2015 Received in revised form 8 May 2015 Accepted 23 May 2015 Available online xxxx
15 16 17 18 19 30
Keywords: Bangladesh Goat Toxoplasma gondii Trans-placental infection
Department of Animal Husbandry and Veterinary Science, Faculty of Agriculture, University of Rajshahi, Rajshahi-6205, Bangladesh Department of Veterinary Parasitology, Faculty of Applied Biological Science, 1-1 Yanagido, Gifu 501-1193, Japan Division of Protozoology, Department of Parasitology, National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjuku-ku, Tokyo 162-8640, Japan
i n f o
a b s t r a c t
We investigated the presence of antibodies against Toxoplasma gondii in domesticated goats intended for human consumption in a rural suburb of Rajshahi, Bangladesh. Antibodies to T. gondii were found in 55.1% (80/145) of the goats tested in our sample. The seroprevalence among goats aged b 1 year, 1–2 years, 2–3 years and ≥ 3 years were 36.7%, 66.0%, 59.1% and 100%, respectively. Our results demonstrated that seroprevalence increased with age. Among the seropositive goats, a subsample of eight free-ranging female goats with access to male goats was placed under continuous observation. During the observation period, these seropositive female goats delivered 11 kids, all of which were found to be seronegative before suckling colostrum. This finding strongly suggested that trans-placental infection rarely occurs in female goats that have acquired an infection before pregnancy. Our results indicate that infection via ingestion of oocysts plays a more important role than endogenous trans-placental infection in maintaining the endemicity of T. gondii among goats in Bangladesh. © 2015 Published by Elsevier Ireland Ltd.
E
34 32 31
43 44 45 46 47 48 49 50 51 52 53 54
R
R
41 42
N C O
39 40
Toxoplasma gondii is a zoonotic protozoan parasite that causes infection in both humans and domestic animals and has a widespread global distribution. Although most infections in humans are asymptomatic, T. gondii is known to cause severe disease in unborn fetuses and immunocompromised patients. Ingestion of tissue cysts in contaminated meat products, ingestion of oocysts shed in cat feces, and transplacental infection are common routes of transmission to humans. It has been reported that 30–63% of human infections in Europe can be attributed to the consumption of undercooked meat [1]. Consumption of meat products produced from carcasses of chronically infected domestic animals is a major risk factor for human T. gondii infection. To prevent its transmission to the human population, therefore, it is necessary to determine the routes of infection of T. gondii in domestic ruminants destined for human consumption and to minimize prevalence of infection among these animals. Although the primary routes of infection in ruminants are ingestion of oocysts shed by cats and trans-placental infection from dams [2], it has yet to be determined which is the most significant route of transmission. While trans-placental transmission of T. gondii to human fetuses only rarely occurs in chronically infected women who had
U
37 38
E
33 35 36
20 21 22 23 24 25 26 27 28 29
C
c
T
b
R O
3
Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats
P
2Q2
Short communication
D
1
⁎ Corresponding author. E-mail addresses: [email protected] (M. Rahman), [email protected] (M. Alauddin), [email protected] (K.M.M. Hossain), [email protected] (M.H. Islam), [email protected] (K. Kitoh), [email protected] (K. Nagamune), [email protected] (Y. Takashima).
acquired their infection before pregnancy (endogenous transplacental infection) [3], the great majority of cases occur in women who had acquired a primary infection during gestation (exogenous trans-placental infection) [4]. In contrast to human toxoplasmosis, quiescent tissue cysts of N. caninum, a closely related species, have been shown to be reactivated during pregnancy and to cause endogenous trans-placental infection in latently infected cows [5,6]. Despite these findings, it remains controversial whether endogenous vertical transmission of T. gondii also occurs in ruminants. Significant familial differences in the frequency of T. gondii infection have been observed in sheep reared within a flock, suggesting endogenous trans-placental infection [7,8]. Although earlier work from the United Kingdom has shown that no newborn lambs delivered by a sample of 31 latently infected dams presented any evidence of trans-placental infection [9], the frequency of endogenous trans-placental T. gondii infection in goats has yet to be determined. However, we have recently shown in a previous study that there was a high seroprevalence of T. gondii among domesticated goats in rural areas of Bangladesh [10,11]. The objective of the present study was to assess the importance of endogenous trans-placental infection for maintaining the endemicity of T. gondii among populations of domesticated goats. To accomplish this, we investigated the prevalence and dynamics of antibodies against T. gondii in goats in Bangladesh by collecting serum samples from 155 goats from 12 domestic farms in a rural suburb of Rajshahi, Bangladesh in March 2014. Because of the subsistence nature of agriculture in this setting, intensive livestock farming is not common, with
http://dx.doi.org/10.1016/j.parint.2015.05.015 1383-5769/© 2015 Published by Elsevier Ireland Ltd.
Please cite this article as: M. Rahman, et al., Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats, Parasitology International (2015), http://dx.doi.org/10.1016/j.parint.2015.05.015
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80
106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122
17KB 17KG⁎,b 18K⁎,b
18 52 221 306
355 K
t1:4
Kid
Month of delivery
At birth⁎,a
1st month
2nd month
3rd month
t1:5 t1:6
Sep. 2014
1024
Sep. 2014 Sep. 2014
64 32
Sep. 2014 Oct. 2014
1024 256
Oct. 2014 June 2014 Sep. 2014
256 32 32
b16 b16 b16 b16 b16 b16 b16 b16 b16 b16 b16
512 64 b16 64 64 1024 16 16 b16 – 128
b16 – – 16 16 32 32 b16 16 – 32
b16 – – b16 b16 16 16 b16 16 – 64
t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17
O
341 354 355
52K 52KF 221K 306M1 306M2 341K 354K⁎,b
t1:3
Antibody titer Dam
F
17
Delivery Kid
Bold type: seropositive. a Serum samples were collected before suckling colostrum. b These kids died during the observation period.
t1:18 t1:19 t1:20
The temporary positive seroconversion observed in the four kids is likely to be due to passive immunization by colostrum immunoglobulin. One kid (I.D. 17KG) died accidentally during the first month. Although we could not directly ascertain the cause of death, its owner reported that it had died by twisting its neck in the dam's tether rope. Another kid (I.D. 355K) remained seropositive until the end of observation period. Considering that this kid was seronegative at the moment of its delivery, it is likely that infection was caused by ingestion of oocysts during the following month. Our observations suggest endogenous trans-placental infection of T. gondii is not common in domesticated goats in rural Bangladesh. Although previous studies in the United Kingdom [7,8] have reported that trans-placental vertical infection is likely to be the primary route of T. gondii infection among ruminants, these made no distinction between exogenous and endogenous transplacental infection. The observations of apparent vertical transmission in these studies may therefore be due to the exogenous transplacental infection from dams that had become infected during gestation through ingestion of oocysts. Taken together, our results and evidence from previous work indicate that ingestion of oocysts plays an important role in maintaining endemicity of T. gondii among goats. Removal of chronically infected female goats from the breeding population may therefore be an ineffective method for eradication of T. gondii among livestock. Prevention of acquired infections, however, should be considered essential as it is likely to represent a more effective approach for controlling T. gondii among domesticated goats. Given that it is unrealistic to control outdoor movements of cats in this setting, the introduction of intensive rearing systems and erection of fences to prevent livestock destined for human consumption coming into contact with infected stray cats is likely to represent a more suitable approach for controlling T. gondii. In this study, neither abortion nor stillbirth was observed. However, it may be possible that fetal infection occurring in early gestation period leads to embryonic demise where only an uninfected kid can be born. Further study to evaluate the risk of fetal death in T. gondii infected female goats is still necessary.
123
Acknowledgments
159
This research was conducted under a consignment agreement between the Food Safety Commission of Japan and the project for food safety risk assessments on 1202, and was partially supported by the Ministry of Education, Culture, Sports, Science and Technology, Grants-in-Aid for Scientific Research (B), 26304040.
160 161
R O
104 105
Dam
P
102 103
I.D.
D
100 101
t1:1 Q1 t1:2
Table 1 Antibody titer in kids born from seropositive dams.
T
98 99
C
96 97
E
94 95
R
92 93
R
90 91
O
88 89
100
C
87
78.5
80
60
100
79.3
N
85 86
U
83 84
farmers typically keeping only a few goats in free-ranging conditions. The sampling procedure was approved by the Animal Research Committee of Gifu University and was carried out with the owners' consent. Testing for T. gondii antibodies was performed using a commercially available diagnostic kit for humans, Toxotest-MT (Eiken Kagaku, Japan), a system which detects anti-Toxoplasma antibodies using a latex agglutination assay. Although this diagnostic kit has been approved for diagnosis of human cases, it was confirmed that the same cut-off value (1:32) used for determining seropositivity is also applicable to goats [12]. Under these criteria, 80/145 goats (55.1%) were found to be seropositive. Although seroprevalence in females is higher than that in males (43/75 and 37/70, respectively), the difference was not significant. After categorizing goats by age, we found that the percentage of seroprevalence of T. gondii among goats aged b1 year, 1–2 years, 2–3 years and ≥ 3 years was 36.7% (22/60), 66.0% (35/53), 59.1% (13/22) and 100% (10/10) respectively. Similar to findings we have reported in a previous study, and as shown in Fig. 1, seroprevalence was found to increase with age [11]. These results strongly suggest that acquired T. gondii infection is common among domesticated goats in rural Bangladesh. However, our finding that goats aged b1 year old also showed relatively high seroprevalence (Fig. 1) prompted us to examine whether endogenous trans-placental infection is a frequent occurrence in domesticated goats. Following identification of seropositive goats in March 2014 using serodiagnosis, we placed a sub-sample of eight free-ranging female goats with access to males under continuous observation. During the observation period, these seropositive female goats delivered a total of 11 kids. Neither abortion nor stillbirth was not observed. Given that the length of gestation is 5 months and that serodiagnosis was carried out in March 2014, the implication is that all dams except one (I.D. 354) had been infected before pregnancy. It was unclear whether another dam (I.D. 354) was infected before or during pregnancy because it had delivered a kid in June 2014 just 3 months after it was shown to be seropositive. As shown in Table 1, all 11 newborn kids were found to be seronegative before suckling colostrum. Since previous studies have reported that goats and sheep that had acquired T. gondii infection before delivery produced specific antibodies against T. gondii before birth [13,14], our results strongly suggest that trans-placental infection had not occurred in our sample. This implies that endogenous trans-placental infection of T. gondii may only rarely occur in goats if at all. Although six kids showed evidence of positive seroconversion after 1 month following delivery, four showed negative seroconversion during the subsequent three months (Table 1).
Seroprevalence (%)
81 82
M. Rahman et al. / Parasitology International xxx (2015) xxx–xxx
E
2
69.2
50.1
51.7
40
36.4 20
124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 Q5 157 158
24.6
<1 year
1−2 years
2−3 years
≥3 years
Age category Fig. 1. Age-specific seroprevalence of T. gondii among the sample of 155 goats tested with 95% confidence intervals (obtained using F distributions) are shown for seroprevalence in each age category.
Please cite this article as: M. Rahman, et al., Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats, Parasitology International (2015), http://dx.doi.org/10.1016/j.parint.2015.05.015
162 163 164
M. Rahman et al. / Parasitology International xxx (2015) xxx–xxx
[1] A.J. Cook, R.E. Gilbert, W. Bufolano, J. Zufferey, E. Petersen, P.A. Jenum, W. Foulon, A.E. Semprini, D.T. Dunn, Sources of Toxoplasma infection in pregnant women: European multicentre case–control study. European research network on congenital toxoplasmosis, BMJ 321 (2000) 142–147. [2] G. Hide, O. Gerwash, E.K. Morley, R.H. Williams, J.M. Hughes, D. Thomasson, M.S. Elmahaishi, K.H. Elmahaishi, R.S. Terry, J.E. Smith, Does vertical transmission contribute to the prevalence of toxoplasmosis? Parasitologia 49 (2007) 223–226. [3] A.J. Trees, D.J. Williams, Endogenous and exogenous transplacental infection in Neospora caninum and Toxoplasma gondii, Trends Parasitol. 21 (2005) 558–561. [4] J.G. Montoya, J.S. Remington, Management of Toxoplasma gondii infection during pregnancy, Clin. Infect. Dis. 47 (4) (2008) 554–566. [5] C.S. Guy, D.J.L. Williams, D.F. Kelly, J.W. McGarry, F. Guy, C. Björkman, R.F. Smith, A.J. Trees, Neospora caninum in persistently infected, pregnant cows: spontaneous transplacental infection is associated with an acute increase in maternal antibody, Vet. Rec. 149 (2001) 443–449. [6] D.J. Williams, C.S. Hartley, C. Björkman, A.J. Trees, Endogenous and exogenous transplacental transmission of Neospora caninum — how the route of transmission impacts on epidemiology and control of disease, Parasitology 136 (2009) 1895–1900. [7] E.K. Morley, R.H. Williams, J.M. Hughes, R.S. Terry, P. Duncanson, J.E. Smith, G. Hide, Significant familial differences in the frequency of abortion and Toxoplasma gondii infection within a flock of Charollais sheep, Parasitology 131 (2005) 181–185.
F
166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186
[8] R.H. Williams, E.K. Morley, J.M. Hughes, P. Duncanson, R.S. Terry, J.E. Smith, G. Hide, High levels of congenital transmission of Toxoplasma gondii in longitudinal and cross-sectional studies on sheep farms provides evidence of vertical transmission in ovine hosts, Parasitology 130 (2005) 301–307. [9] S.M. Rodger, S.W. Maley, S.E. Wright, A. Mackellar, F. Wesley, J. Sales, D. Buxton, Role of endogenous transplacental transmission in toxoplasmosis in sheep, Vet. Rec. 159 (2006) 768–772. [10] M.D. Shahiduzzaman, M.D.R. Islam, M.M. Khatun, T. Batanova, K. Kitoh, Y. Takashima, Toxoplasma gondii seroprevalence in domestic animals and humans in Mymensingh District, Bangladesh, J. Vet. Med. Sci. 73 (2011) 1375–1376. [11] M. Rahman, M.T. Azad, S.M. Rouf, K. Ohya, S.P. Chiou, B. Baba, K. Kitoh, Y. Takashima, Age-specificity of Toxoplasma gondii seroprevalence in sheep, goats and cattle on subsistence farms in Bangladesh, J. Vet. Med. Sci. 76 (2014) 1257–1259. [12] H. Kyan, M. Taira, A. Yamamoto, C. Inaba, S. Zakimi, Isolation and characterization of Toxoplasma gondii genotypes from goats at an abattoir in Okinawa, Jpn. J. Infect. Dis. 65 (2012) 167–170. [13] J.P. Dubey, S. Miller, G. Desmonts, P. Thulliez, W.R. Anderson, Toxoplasma gondiiinduced abortion in dairy goats, J. Am. Vet. Med. Assoc. 188 (1986) 159–162. [14] P.X. Marques, J. O'Donovan, E.J. Williams, J. Gutierrez, S. Worrall, M. McElroy, A. Proctor, C. Brady, D. Sammin, H. Bassett, D. Buxton, S. Maley, B.K. Markey, J.E. Nally, Detection of Toxoplasma gondii antigens reactive with antibodies from serum, amniotic, and allantoic fluids from experimentally infected pregnant ewes, Vet. Parasitol. 185 (2012) 91–100.
References
O
165
3
U
N C O
R
R
E
C
T
E
D
P
R O
210
Please cite this article as: M. Rahman, et al., Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats, Parasitology International (2015), http://dx.doi.org/10.1016/j.parint.2015.05.015
187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209
Contents lists available at ScienceDirect
Parasitology International journal homepage: www.elsevier.com/locate/parint
5
F
Moizur Rahman a, Md. Alauddin a, K.M. Mozaffor Hossain a, Md. Hemayetul Islam a, Katsuya Kitoh b, Kisaburo Nagamune c, Yasuhiro Takashima b,⁎
O
4Q3
6 7 8Q4
a
9
a r t i c l e
10 11 12 13 14
Article history: Received 17 February 2015 Received in revised form 8 May 2015 Accepted 23 May 2015 Available online xxxx
15 16 17 18 19 30
Keywords: Bangladesh Goat Toxoplasma gondii Trans-placental infection
Department of Animal Husbandry and Veterinary Science, Faculty of Agriculture, University of Rajshahi, Rajshahi-6205, Bangladesh Department of Veterinary Parasitology, Faculty of Applied Biological Science, 1-1 Yanagido, Gifu 501-1193, Japan Division of Protozoology, Department of Parasitology, National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjuku-ku, Tokyo 162-8640, Japan
i n f o
a b s t r a c t
We investigated the presence of antibodies against Toxoplasma gondii in domesticated goats intended for human consumption in a rural suburb of Rajshahi, Bangladesh. Antibodies to T. gondii were found in 55.1% (80/145) of the goats tested in our sample. The seroprevalence among goats aged b 1 year, 1–2 years, 2–3 years and ≥ 3 years were 36.7%, 66.0%, 59.1% and 100%, respectively. Our results demonstrated that seroprevalence increased with age. Among the seropositive goats, a subsample of eight free-ranging female goats with access to male goats was placed under continuous observation. During the observation period, these seropositive female goats delivered 11 kids, all of which were found to be seronegative before suckling colostrum. This finding strongly suggested that trans-placental infection rarely occurs in female goats that have acquired an infection before pregnancy. Our results indicate that infection via ingestion of oocysts plays a more important role than endogenous trans-placental infection in maintaining the endemicity of T. gondii among goats in Bangladesh. © 2015 Published by Elsevier Ireland Ltd.
E
34 32 31
43 44 45 46 47 48 49 50 51 52 53 54
R
R
41 42
N C O
39 40
Toxoplasma gondii is a zoonotic protozoan parasite that causes infection in both humans and domestic animals and has a widespread global distribution. Although most infections in humans are asymptomatic, T. gondii is known to cause severe disease in unborn fetuses and immunocompromised patients. Ingestion of tissue cysts in contaminated meat products, ingestion of oocysts shed in cat feces, and transplacental infection are common routes of transmission to humans. It has been reported that 30–63% of human infections in Europe can be attributed to the consumption of undercooked meat [1]. Consumption of meat products produced from carcasses of chronically infected domestic animals is a major risk factor for human T. gondii infection. To prevent its transmission to the human population, therefore, it is necessary to determine the routes of infection of T. gondii in domestic ruminants destined for human consumption and to minimize prevalence of infection among these animals. Although the primary routes of infection in ruminants are ingestion of oocysts shed by cats and trans-placental infection from dams [2], it has yet to be determined which is the most significant route of transmission. While trans-placental transmission of T. gondii to human fetuses only rarely occurs in chronically infected women who had
U
37 38
E
33 35 36
20 21 22 23 24 25 26 27 28 29
C
c
T
b
R O
3
Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats
P
2Q2
Short communication
D
1
⁎ Corresponding author. E-mail addresses: [email protected] (M. Rahman), [email protected] (M. Alauddin), [email protected] (K.M.M. Hossain), [email protected] (M.H. Islam), [email protected] (K. Kitoh), [email protected] (K. Nagamune), [email protected] (Y. Takashima).
acquired their infection before pregnancy (endogenous transplacental infection) [3], the great majority of cases occur in women who had acquired a primary infection during gestation (exogenous trans-placental infection) [4]. In contrast to human toxoplasmosis, quiescent tissue cysts of N. caninum, a closely related species, have been shown to be reactivated during pregnancy and to cause endogenous trans-placental infection in latently infected cows [5,6]. Despite these findings, it remains controversial whether endogenous vertical transmission of T. gondii also occurs in ruminants. Significant familial differences in the frequency of T. gondii infection have been observed in sheep reared within a flock, suggesting endogenous trans-placental infection [7,8]. Although earlier work from the United Kingdom has shown that no newborn lambs delivered by a sample of 31 latently infected dams presented any evidence of trans-placental infection [9], the frequency of endogenous trans-placental T. gondii infection in goats has yet to be determined. However, we have recently shown in a previous study that there was a high seroprevalence of T. gondii among domesticated goats in rural areas of Bangladesh [10,11]. The objective of the present study was to assess the importance of endogenous trans-placental infection for maintaining the endemicity of T. gondii among populations of domesticated goats. To accomplish this, we investigated the prevalence and dynamics of antibodies against T. gondii in goats in Bangladesh by collecting serum samples from 155 goats from 12 domestic farms in a rural suburb of Rajshahi, Bangladesh in March 2014. Because of the subsistence nature of agriculture in this setting, intensive livestock farming is not common, with
http://dx.doi.org/10.1016/j.parint.2015.05.015 1383-5769/© 2015 Published by Elsevier Ireland Ltd.
Please cite this article as: M. Rahman, et al., Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats, Parasitology International (2015), http://dx.doi.org/10.1016/j.parint.2015.05.015
55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80
106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122
17KB 17KG⁎,b 18K⁎,b
18 52 221 306
355 K
t1:4
Kid
Month of delivery
At birth⁎,a
1st month
2nd month
3rd month
t1:5 t1:6
Sep. 2014
1024
Sep. 2014 Sep. 2014
64 32
Sep. 2014 Oct. 2014
1024 256
Oct. 2014 June 2014 Sep. 2014
256 32 32
b16 b16 b16 b16 b16 b16 b16 b16 b16 b16 b16
512 64 b16 64 64 1024 16 16 b16 – 128
b16 – – 16 16 32 32 b16 16 – 32
b16 – – b16 b16 16 16 b16 16 – 64
t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17
O
341 354 355
52K 52KF 221K 306M1 306M2 341K 354K⁎,b
t1:3
Antibody titer Dam
F
17
Delivery Kid
Bold type: seropositive. a Serum samples were collected before suckling colostrum. b These kids died during the observation period.
t1:18 t1:19 t1:20
The temporary positive seroconversion observed in the four kids is likely to be due to passive immunization by colostrum immunoglobulin. One kid (I.D. 17KG) died accidentally during the first month. Although we could not directly ascertain the cause of death, its owner reported that it had died by twisting its neck in the dam's tether rope. Another kid (I.D. 355K) remained seropositive until the end of observation period. Considering that this kid was seronegative at the moment of its delivery, it is likely that infection was caused by ingestion of oocysts during the following month. Our observations suggest endogenous trans-placental infection of T. gondii is not common in domesticated goats in rural Bangladesh. Although previous studies in the United Kingdom [7,8] have reported that trans-placental vertical infection is likely to be the primary route of T. gondii infection among ruminants, these made no distinction between exogenous and endogenous transplacental infection. The observations of apparent vertical transmission in these studies may therefore be due to the exogenous transplacental infection from dams that had become infected during gestation through ingestion of oocysts. Taken together, our results and evidence from previous work indicate that ingestion of oocysts plays an important role in maintaining endemicity of T. gondii among goats. Removal of chronically infected female goats from the breeding population may therefore be an ineffective method for eradication of T. gondii among livestock. Prevention of acquired infections, however, should be considered essential as it is likely to represent a more effective approach for controlling T. gondii among domesticated goats. Given that it is unrealistic to control outdoor movements of cats in this setting, the introduction of intensive rearing systems and erection of fences to prevent livestock destined for human consumption coming into contact with infected stray cats is likely to represent a more suitable approach for controlling T. gondii. In this study, neither abortion nor stillbirth was observed. However, it may be possible that fetal infection occurring in early gestation period leads to embryonic demise where only an uninfected kid can be born. Further study to evaluate the risk of fetal death in T. gondii infected female goats is still necessary.
123
Acknowledgments
159
This research was conducted under a consignment agreement between the Food Safety Commission of Japan and the project for food safety risk assessments on 1202, and was partially supported by the Ministry of Education, Culture, Sports, Science and Technology, Grants-in-Aid for Scientific Research (B), 26304040.
160 161
R O
104 105
Dam
P
102 103
I.D.
D
100 101
t1:1 Q1 t1:2
Table 1 Antibody titer in kids born from seropositive dams.
T
98 99
C
96 97
E
94 95
R
92 93
R
90 91
O
88 89
100
C
87
78.5
80
60
100
79.3
N
85 86
U
83 84
farmers typically keeping only a few goats in free-ranging conditions. The sampling procedure was approved by the Animal Research Committee of Gifu University and was carried out with the owners' consent. Testing for T. gondii antibodies was performed using a commercially available diagnostic kit for humans, Toxotest-MT (Eiken Kagaku, Japan), a system which detects anti-Toxoplasma antibodies using a latex agglutination assay. Although this diagnostic kit has been approved for diagnosis of human cases, it was confirmed that the same cut-off value (1:32) used for determining seropositivity is also applicable to goats [12]. Under these criteria, 80/145 goats (55.1%) were found to be seropositive. Although seroprevalence in females is higher than that in males (43/75 and 37/70, respectively), the difference was not significant. After categorizing goats by age, we found that the percentage of seroprevalence of T. gondii among goats aged b1 year, 1–2 years, 2–3 years and ≥ 3 years was 36.7% (22/60), 66.0% (35/53), 59.1% (13/22) and 100% (10/10) respectively. Similar to findings we have reported in a previous study, and as shown in Fig. 1, seroprevalence was found to increase with age [11]. These results strongly suggest that acquired T. gondii infection is common among domesticated goats in rural Bangladesh. However, our finding that goats aged b1 year old also showed relatively high seroprevalence (Fig. 1) prompted us to examine whether endogenous trans-placental infection is a frequent occurrence in domesticated goats. Following identification of seropositive goats in March 2014 using serodiagnosis, we placed a sub-sample of eight free-ranging female goats with access to males under continuous observation. During the observation period, these seropositive female goats delivered a total of 11 kids. Neither abortion nor stillbirth was not observed. Given that the length of gestation is 5 months and that serodiagnosis was carried out in March 2014, the implication is that all dams except one (I.D. 354) had been infected before pregnancy. It was unclear whether another dam (I.D. 354) was infected before or during pregnancy because it had delivered a kid in June 2014 just 3 months after it was shown to be seropositive. As shown in Table 1, all 11 newborn kids were found to be seronegative before suckling colostrum. Since previous studies have reported that goats and sheep that had acquired T. gondii infection before delivery produced specific antibodies against T. gondii before birth [13,14], our results strongly suggest that trans-placental infection had not occurred in our sample. This implies that endogenous trans-placental infection of T. gondii may only rarely occur in goats if at all. Although six kids showed evidence of positive seroconversion after 1 month following delivery, four showed negative seroconversion during the subsequent three months (Table 1).
Seroprevalence (%)
81 82
M. Rahman et al. / Parasitology International xxx (2015) xxx–xxx
E
2
69.2
50.1
51.7
40
36.4 20
124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 Q5 157 158
24.6
<1 year
1−2 years
2−3 years
≥3 years
Age category Fig. 1. Age-specific seroprevalence of T. gondii among the sample of 155 goats tested with 95% confidence intervals (obtained using F distributions) are shown for seroprevalence in each age category.
Please cite this article as: M. Rahman, et al., Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats, Parasitology International (2015), http://dx.doi.org/10.1016/j.parint.2015.05.015
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[1] A.J. Cook, R.E. Gilbert, W. Bufolano, J. Zufferey, E. Petersen, P.A. Jenum, W. Foulon, A.E. Semprini, D.T. Dunn, Sources of Toxoplasma infection in pregnant women: European multicentre case–control study. European research network on congenital toxoplasmosis, BMJ 321 (2000) 142–147. [2] G. Hide, O. Gerwash, E.K. Morley, R.H. Williams, J.M. Hughes, D. Thomasson, M.S. Elmahaishi, K.H. Elmahaishi, R.S. Terry, J.E. Smith, Does vertical transmission contribute to the prevalence of toxoplasmosis? Parasitologia 49 (2007) 223–226. [3] A.J. Trees, D.J. Williams, Endogenous and exogenous transplacental infection in Neospora caninum and Toxoplasma gondii, Trends Parasitol. 21 (2005) 558–561. [4] J.G. Montoya, J.S. Remington, Management of Toxoplasma gondii infection during pregnancy, Clin. Infect. Dis. 47 (4) (2008) 554–566. [5] C.S. Guy, D.J.L. Williams, D.F. Kelly, J.W. McGarry, F. Guy, C. Björkman, R.F. Smith, A.J. Trees, Neospora caninum in persistently infected, pregnant cows: spontaneous transplacental infection is associated with an acute increase in maternal antibody, Vet. Rec. 149 (2001) 443–449. [6] D.J. Williams, C.S. Hartley, C. Björkman, A.J. Trees, Endogenous and exogenous transplacental transmission of Neospora caninum — how the route of transmission impacts on epidemiology and control of disease, Parasitology 136 (2009) 1895–1900. [7] E.K. Morley, R.H. Williams, J.M. Hughes, R.S. Terry, P. Duncanson, J.E. Smith, G. Hide, Significant familial differences in the frequency of abortion and Toxoplasma gondii infection within a flock of Charollais sheep, Parasitology 131 (2005) 181–185.
F
166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186
[8] R.H. Williams, E.K. Morley, J.M. Hughes, P. Duncanson, R.S. Terry, J.E. Smith, G. Hide, High levels of congenital transmission of Toxoplasma gondii in longitudinal and cross-sectional studies on sheep farms provides evidence of vertical transmission in ovine hosts, Parasitology 130 (2005) 301–307. [9] S.M. Rodger, S.W. Maley, S.E. Wright, A. Mackellar, F. Wesley, J. Sales, D. Buxton, Role of endogenous transplacental transmission in toxoplasmosis in sheep, Vet. Rec. 159 (2006) 768–772. [10] M.D. Shahiduzzaman, M.D.R. Islam, M.M. Khatun, T. Batanova, K. Kitoh, Y. Takashima, Toxoplasma gondii seroprevalence in domestic animals and humans in Mymensingh District, Bangladesh, J. Vet. Med. Sci. 73 (2011) 1375–1376. [11] M. Rahman, M.T. Azad, S.M. Rouf, K. Ohya, S.P. Chiou, B. Baba, K. Kitoh, Y. Takashima, Age-specificity of Toxoplasma gondii seroprevalence in sheep, goats and cattle on subsistence farms in Bangladesh, J. Vet. Med. Sci. 76 (2014) 1257–1259. [12] H. Kyan, M. Taira, A. Yamamoto, C. Inaba, S. Zakimi, Isolation and characterization of Toxoplasma gondii genotypes from goats at an abattoir in Okinawa, Jpn. J. Infect. Dis. 65 (2012) 167–170. [13] J.P. Dubey, S. Miller, G. Desmonts, P. Thulliez, W.R. Anderson, Toxoplasma gondiiinduced abortion in dairy goats, J. Am. Vet. Med. Assoc. 188 (1986) 159–162. [14] P.X. Marques, J. O'Donovan, E.J. Williams, J. Gutierrez, S. Worrall, M. McElroy, A. Proctor, C. Brady, D. Sammin, H. Bassett, D. Buxton, S. Maley, B.K. Markey, J.E. Nally, Detection of Toxoplasma gondii antigens reactive with antibodies from serum, amniotic, and allantoic fluids from experimentally infected pregnant ewes, Vet. Parasitol. 185 (2012) 91–100.
References
O
165
3
U
N C O
R
R
E
C
T
E
D
P
R O
210
Please cite this article as: M. Rahman, et al., Prevalence and dynamics of antibodies against Toxoplasma gondii in kids born from naturally infected goats, Parasitology International (2015), http://dx.doi.org/10.1016/j.parint.2015.05.015
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