|Year : 2019 | Volume
| Issue : 3 | Page : 351-357
Seroprevalence of Toxoplasmosis at a Tertiary Care Centre in North India from 2004 to 2014
Abhishek Mewara, Shreya Singh, Sumeeta Khurana, Parakriti Gupta, Rakesh Sehgal
Department of Medical Parasitology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
|Date of Submission||04-Sep-2019|
|Date of Decision||02-Nov-2019|
|Date of Acceptance||03-Dec-2019|
|Date of Web Publication||29-Jan-2020|
Dr. Sumeeta Khurana
Department of Medical Parasitology, Postgraduate Institute of Medical Education and Research, Chandigarh - 160 012
Source of Support: None, Conflict of Interest: None
Purpose: This study was carried out to determine the seroprevalence of anti-Toxoplasma gondii antibodies in different groups of patients at a tertiary care hospital in North India. Materials and Methods: Clinical and demographic data such as age and gender of patients who had undergone testing for the presence of anti-T. gondii IgG and IgM antibodies between January 2004 and October 2014 were retrospectively analysed. Results: Amongst the 8397 serum samples, an overall seropositivity of 21% (n = 1763) and IgG and IgM seropositivity of 5.7% (n = 481) and 15.3% (n = 1282) were respectively observed. Compared to the period of 2004–2012 (median seroprevalence: 23.6%), a decline in seropositivity to 9.7% in 2013 and 8.1% in 2014 was noted. A rising seroprevalence with age and a higher seroprevalence in females versus males (29.5%, n = 1179 vs. 13.3%, n = 584) were recorded. The highest seroprevalence was observed in suspected ocular toxoplasmosis (47.2%, n = 47), followed by neurological (26.8%, n = 77), human immunodeficiency virus/acquired immunodeficiency syndrome (18.9%, n = 267), post-transplant (17.1%, n = 12) and congenital (7.2%, n = 144) toxoplasmosis. In patients screened for Toxoplasma exposure, the seropositivity was 47.8% (n = 11) in transplant screening and 44.9% (n = 781) in antenatal screening. Conclusion: Toxoplasma infection is highly prevalent in the population of North India across various clinical categories of patients. Future studies focusing on continuous monitoring of seroprevalence trends and elucidation of the risk factors associated with seropositivity in more defined groups of patients are needed.
Keywords: Antenatal screening, human immunodeficiency virus/acquired immunodeficiency syndrome, India, seroprevalence, Toxoplasma gondii
|How to cite this article:|
Mewara A, Singh S, Khurana S, Gupta P, Sehgal R. Seroprevalence of Toxoplasmosis at a Tertiary Care Centre in North India from 2004 to 2014. Indian J Med Microbiol 2019;37:351-7
|How to cite this URL:|
Mewara A, Singh S, Khurana S, Gupta P, Sehgal R. Seroprevalence of Toxoplasmosis at a Tertiary Care Centre in North India from 2004 to 2014. Indian J Med Microbiol [serial online] 2019 [cited 2020 Jul 13];37:351-7. Available from: http://www.ijmm.org/text.asp?2019/37/3/351/277066
| ~ Introduction|| |
Toxoplasmosis is caused by the intracellular, protozoan parasite Toxoplasma gondii and infects nearly one-third of the population worldwide. This disease is primarily transmitted to humans through the ingestion of infected meat, exposure to environmentally resistant oocysts passed in cats faeces and from newly infected pregnant women to the unborn foetus. Despite the usual asymptomatic nature of this infection, significant morbidity is imposed in individuals with impaired immune systems and in congenitally infected children, necessitating the implementation of effective means for its prevention, diagnosis, treatment and improving estimates of disease burden. The diagnosis of toxoplasmosis chiefly relies on the detection of Toxoplasma-specific IgG and IgM antibodies, and Toxoplasma seroprevalence varies according to the patients' geographic location, gender, clinical presentation and immune status.
In India, the seroprevalence of toxoplasmosis is 24.3%, varying from 4.7% to 51.8% in North India to 37.3% in South India.,,, Although the incidence of congenital toxoplasmosis is variable, the acquisition of toxoplasmosis in antenatal period indicated by maternal seroconversion rates is 0.2%–1% in most countries. Nearly, 10%–30% of patients with human immunodeficiency virus/acquired immunodeficiency syndrome (HIV/AIDS) in the United States of America (USA) and 20%–50% in Europe die from toxoplasmosis. A prevalence of up to 50% in transplant recipients, and rising reports of Toxoplasma-related neurological disorders are also concerning. The burden of diseases attributable to toxoplasmosis is probably greater than currently suggested, and seroprevalence data from different patient groups could help in the formulation of targeted health policies. Thus, we analysed Toxoplasma seroprevalence in various patient groups at our tertiary care hospital over more than a decade.
| ~ Materials and Methods|| |
The study was conducted at the Postgraduate Institute of Medical Education and Research (PGIMER), Chandigarh, India, a tertiary care hospital catering to a population of seven neighbouring states, namely Punjab, Haryana, Himachal Pradesh, Uttar Pradesh, Uttarakhand, Jammu and Kashmir and Rajasthan.
The study was approved by the Institute Ethics Committee of PGIMER, Chandigarh (Reference number: NK/5136/Res). Inclusion criteria: All patients samples received in the Medical Parasitology-Serology Laboratory of PGIMER, Chandigarh, India, from January 2004 to October 2014 for Toxoplasma serology were included for the analysis. This included samples from patients with clinical suspicion of toxoplasmosis and those undergoing routine screening (antenatal and transplant donors). Exclusion criteria: All samples haemolysed, improperly labelled, leaking or of inadequate quantity were excluded. The patient details and results of Toxoplasma serology performed throughout the study period were analysed. Amongst a total of 8397 included patients, 6633 patients were clinically suspected of toxoplasmosis and 1764 were subjected to routine screening for antibodies against T. gondii. The patients with clinically suspected toxoplasmosis (n=6633) were further categorized as: congenital toxoplasmosis (n = 2000), neurological toxoplasmosis (n = 287), ocular toxoplasmosis (n = 104), toxoplasmosis in immunocompromised patients and the remaining patients who could not be assigned any clinical category were grouped according to age as paediatric (n = 1946) and adult toxoplasmosis (n = 817). Immunocompromised patients with toxoplasmosis comprised of patients with HIV/AIDS (n = 1409) and post-transplant recipients (n = 70), which included haematopoietic stem cell transplant [HSCT] [n = 64], liver transplant [n = 4] and renal transplant [n = 2] recipients. A total of 1764 samples were subjected to routine screening which included antenatal screening (n = 1741) and transplant donor screening (n = 23) cases. All patients were categorised age wise into neonates (<1 month), infants (>1 month–1 year), 1–5 years, 6–12 years, 13–18 years, 19–30 years, 31–40 years, 41–50 years, 51–60 years, 61–70 years, 71–80 years and 81–90 years for the analysis. A flow diagram depicting the study design is shown in [Figure 1].
For the detection of anti-T. gondii antibodies, blood was aseptically collected by venipuncture in sterile plain vials. The blood was allowed to clot, and following clot retraction, the serum sample was separated and stored at −20°C till further analysis.
All samples were subjected to the in-house enzyme-linked immunosorbent assay (ELISA) for the detection of anti-T. gondii IgG and IgM antibodies as previously reported in the protocol. Briefly, the antigen was prepared from the RH strain of T. gondii tachyzoites harvested from the peritoneal cavity of Swiss albino mice after 3 days of infection. The tachyzoites were purified by differential centrifugation, kept overnight at 4°C and then subjected to sonication and cold centrifugation. Toxoplasma antigen (1 μg/well) was coated on microtitre plates, and ELISA was performed as described previously.
The statistical analysis was done using SPSS software version 19.0 (SPSS South Asia Pvt. Ltd., Bangalore, Karnataka, India).
| ~ Results|| |
Toxoplasma seropositivity from 2004 to 2014
Of the 8397 samples received for Toxoplasma serology, 4400 (52.4%) were from male and 3997 (47.6%) from female patients. An overall seropositivity of 21% (n = 1763/8397) was recorded, with IgG positivity in 5.7% (n = 481/8397) and IgM positivity in 15.3% (n = 1282/8397) patients. Amongst IgM seropositive cases, 28.7% (n = 368/1282) were also IgG positive, whereas 71.3% (n = 914/1282) were IgG negative. The percentage Toxoplasma seroprevalence over the 10-year study duration is depicted in [Figure 2]a. The seroprevalence ranged from 16.4% to 31.7% from 2004 to 2012, whereas a drop to 9.7% and 8.1% was noted in 2013 and 2014, respectively.
|Figure 2: Percentage prevalence of Toxoplasma seropositivity: (a) Overall seropositivity from 2004 to 2014. (b) Total, IgG and IgM seropositivity in different age groups. (c) Total, IgG and IgM seropositivity in different clinical categories|
Click here to view
Age-wise Toxoplasma seroprevalence
With increasing age, a statistically significant increase in overall seropositivity was observed, though there were fluctuations in the intervening years, with the lowest seropositivity in infants (4.9%, n = 73/1480). The highest seropositivity was seen in the 81–90 years' age group (80%, n = 4/5) which included 3 cases of HIV related and one case of neurological toxoplasmosis. Amongst all 1763 samples with positive Toxoplasma serology, the majority belonged to patients in the 19–30 years' age group (47.4%, n = 836), followed by 31–40 years (16.0%, n = 282). Similarly, amongst all 1282 patients with IgM seropositivity, the majority were present in the 19–30 years' age group (53%, n = 680), followed by 31–40 years' age group (n = 198, 15.4%). Majority of the Toxoplasma IgG-seropositive cases were noted in the 19–30 years' age group (32.4%, n = 156/481), followed by 6–12 years (7.7%, n = 37/481) and >1–5 years' age group (5.6%, n = 27/481). Amongst all age groups, IgM seropositivity was higher than IgG seropositivity except for the extremes of ages including neonates (11.4% vs. 2.7%) and elderly of 71–80 years (25% vs. 20%) and 81–90 years (60% vs. 20%) [Figure 2]b and [Table 1].
|Table 1: Percentage seropositivity for Toxoplasma infection with respect to age and gender|
Click here to view
Gender-wise Toxoplasma seroprevalence
A higher Toxoplasma seropositivity was observed in females at 29.5% (n = 1179/3997) compared to males at 13.3% (n = 584/4400). IgM seropositivity was also higher in females versus males at 24% (n = 959) versus 7.3% (n = 323) males, whereas IgG seropositivity was similar across both genders at 5.5% in females (n = 220) and 5.9% in males (n = 261). Across age groups years 19–30 (P = 0.032), 31–40 (P < 0.001) and 41–50 (P = 0.001), a higher seropositivity was revealed amongst female neonates (P = 0.036), as shown in [Table 1].
Toxoplasma seroprevalence in different clinical categories
In patients with clinically suspected toxoplasmosis, the seroprevalence was highest in cases of ocular toxoplasmosis (n = 47/104, 47.2%), followed by neurological toxoplasmosis (n = 77/287, 26.8%), toxoplasmosis in HIV/AIDS (n = 267/1409, 18.9%), toxoplasmosis in post-transplant recipients (n = 12/70, 17.1%) and patients with congenital toxoplasmosis (n = 144/2000, 7.2%). Amongst other cases, adult toxoplasmosis (n = 252/817, 30.8%) showed a higher seroprevalence compared to of paediatric cases (n = 172/1946, 8.8%) [Table 2]. In patients subjected to Toxoplasma screening, the seropositivity was 47.8% (n = 11/23) in transplant screening and 44.9% (n = 781/1741) in antenatal screening cases [Figure 2]c.
|Table 2: Percentage seropositivity for Toxoplasma infection in different clinical categories (2004-2014)|
Click here to view
IgM seropositivity was observed to be maximum in transplant donor screening (n = 10/23, 43.5%), followed by antenatal screening (n = 674/1741, 38.7%), ocular (n = 28/104, 26.9%) and adult toxoplasmosis (n = 170/817, 20.8%), whereas the highest IgG seropositivity rate was observed in patients with ocular toxoplasmosis (n = 19/104, 18.3%), followed by neurological (n = 35/287, 12.2%), adult (n = 82/817, 10%) and HIV/AIDS-associated toxoplasmosis (n = 131/1409, 9.3%) [Figure 2]c. A decline in seroprevalence from 2004 to 2014 was noted in HIV/AIDS patients and antenatal screening group.
| ~ Discussion|| |
Since toxoplasmosis seroprevalence varies with patient demographics and regional socioeconomic parameters, an awareness of the seroprevalence trends in different patient groups provides insights for framing targeted public health policies. We observed an overall seroprevalence of 21% with anti-Toxoplasma IgG in 5.7% and IgM in 15.3% of patients at our hospital in North India. Another recent study from North India evaluating anti-Toxoplasma IgG and IgM antibodies in women of reproductive age group reported a prevalence of 22.4% and 1.4%, respectively. Studies from North India have documented an anti-Toxoplasma IgG seroprevalence of 15%–51.8% and 2%–5% for IgM antibodies.,, Globally, approximately 25%–30% of humans are infected with T. gondii; however, the seroprevalence varies greatly between different countries (10%–80%) and even within countries. This is perhaps due to the differences in exposure to the organism according to the socioeconomic status, cultural beliefs and anthropogenic factors such as handling and owning cats, consumption of meat and unwashed fruits and vegetables, handling soil and variations in hand hygiene practices. Other factors such as climate which affects the survival of oocysts in the environment, sanitation and quality of water supply can also impact the seroprevalence trends. The Toxoplasma seroprevalence in our study revealed a decline from 28.0% in 2004 to 8.1% in 2014, the exact reasons of which need to be explored. It is plausible that an improvement in socioeconomic status, water and food sanitation, better regulation of indigenous, imported meat quality, avoidance of risk factors during pregnancy and increasing awareness of toxoplasmosis amongst patients and doctors could all have contributed to this. A study from Poland investigating the prevalence of anti-Toxoplasma IgG between 1998 and 2003 reported a decline in seroprevalence from 45.4% to 39.4%. The authors of the study attributed this to improvements in T. gondii infection prevention over the years. A decline in maternal seroprevalence from 53% to 20% and a 85% decrease in the incidence of congenital toxoplasmosis over time have also been seen in Switzerland from 1982 to 2015.
The relationship between increased prevalence of Toxoplasma and age has been previously documented in various studies.,, However, most of the studies have been carried out in women of childbearing age. We observed a rising seroprevalence of Toxoplasma across all ages in both men and women, with the highest percentage seropositivity amongst the elderly at 45%–80% in the 60–90 years' age group. From Germany, Wilking et al. 2016 also reported that Toxoplasma seroprevalence increased from 20% in the 18–29 years' age group to 77% in the 70–79 years' age group in both genders. We noted that IgG seropositivity was higher in the extremes of age possibly due to transfer of maternal IgG antibodies in neonates and persisting IgG antibodies in the elderly population.
A higher seroprevalence amongst females, particularly in the fertile age group of 19–50 years, was seen, although a higher seroprevalence with age was not evident. Toxoplasma-specific IgG seroprevalence amongst women and the infection pressure, or probability of exposure to T. gondii, have been reported to increase with age in previous studies.,
The seroprevalence of Toxoplasma amongst suspected congenital toxoplasmosis cases was 7.2% in our study. Congenital toxoplasmosis can result in abortion or lead to severe visual and neurological malformation in the foetus such as hydrocephalus, cerebral calcification and/or chorioretinitis., In France, early detection of seroconversion in pregnant women, frequent re-testing using highly sensitive polymerase chain reaction, followed by early treatment in the national program, has been associated with a lower rate of severe congenital toxoplasmosis. Recent reports of high prevalence of congenital toxoplasmosis (28%) from Brazil, suggest that screening programs could be beneficial in such regions.
There is a low-to-moderate prevalence of Toxoplasma infection reported in India amongst antenatal women ranging from 15% to 49.5%, and was also observed to be 44.9% in our study. A low seroprevalence (10%–30%) is reported from developed regions such as North America, northern Europe and Japan, whereas a moderate seroprevalence (30%–50%) has been reported from central and southern Europe, and high seroprevalence (>50%) has been found in Latin America and African countries. Routine antenatal screening is practised at our tertiary care centre; however, it is not a norm at the rural primary healthcare centres and other district-based hospitals of the country, and a higher prevalence of pregnancy-associated toxoplasmosis can be expected in the community.
Amongst other clinical categories of patients, the highest seropositivity was observed in patients with suspected ocular toxoplasmosis. Although congenital infections commonly cause retinochoroiditis, most cases of ocular toxoplasmosis are acquired after birth, and it is an important cause of visual impairment. A prevalence of Toxoplasma ranging from 4.2% to 8.4% has been described in cases of uveitis in various studies; however, most studies have used molecular tests for defining cases. Toxoplasmosis serology is useful to confirm active toxoplasmosis retinochoroiditis and supports clinical diagnosis in up to 96% of cases. In 80% of the immunocompetent patients, no clinical signs of toxoplasmosis are apparent; therefore, assessing the serological status is essential in cases at high risk for more severe disease forms such as ocular toxoplasmosis.
The incidence of opportunist toxoplasmosis is probably underestimated, poorly studied and depends on the seroprevalence of infection amongst the general population. It carries the risk of complications in HIV/AIDS patients and recipients of HSCT or SOT, wherein Toxoplasma-naïve patients are at a higher risk of acute, severe and lethal toxoplasmosis, whereas patients with latent infection are at a risk of reactivation and secondary dissemination. We observed an 18.9% seroprevalence of Toxoplasma amongst HIV/AIDS patients and 17.1% in post-transplant recipients. Serology is often limited due to immune deficiency impacting antibody production, making molecular detection of parasite the most sensitive test in these settings. Pre-transplant screening of donors and recipients also revealed a high seroprevalence (47.8%). However, the true burden of toxoplasmosis in this patient group can only be estimated by screening paired pre- and post- transplant samples from both donors and recipients. Since this was not performed in the present study, future studies must be undertaken to elucidate the same. In addition, a decline in seroprevalence was noted from 2004 to 2014 amongst antenatal cases (48.7% vs. 19.7%) and HIV/AIDS patients (22.2% vs. 4.7%), the reasons of which are not clear, but could be indicative of improvements in T. gondii infection prevention in HIV/AIDS patients and better awareness amongst physicians regarding antenatal screening and management of toxoplasmosis in these patient groups. In a recent study examining HIV-infected military personnel screened for T. gondii IgG antibody in the USA over 30 years, a decline in seroprevalence was observed which the authors suggested was due to a possible decreased exposure to the infectious agent as a result of ongoing public health education, improved hygiene and general improvements related to meat preparation and handling of soil and cat faeces. Unfortunately, in our study, some patient details such as contact with pets, feeding habits, history of previous medication and blood transfusions were not available, and thus, the factors affecting seroprevalence could not be studied.
| ~ Conclusion|| |
The epidemiology of toxoplasmosis is complex and involves many variables. To adequately understand the factors associated with this infection further studies in seropositive individuals with focus on risk assessment are required. The serial monitoring of seroconversion trends in specific patient populations such as HIV/AIDS and transplant recipients could also important insights into disease epidemiology.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| ~ References|| |
Saadatnia G, Golkar M. A review on human toxoplasmosis. Scand J Infect Dis 2012;44:805-14.
Hill D, Dubey JP. Toxoplasma gondii: Transmission, diagnosis and prevention. Clin Microbiol Infect 2002;8:634-40.
Khurana S, Bagga R, Aggarwal A, Lyngdoh V, Shivapriya, Diddi K, et al
. Serological screening for antenatal toxoplasma infection in India. Indian J Med Microbiol 2010;28:143-6.
] [Full text]
Dhumne M, Sengupta C, Kadival G, Rathinaswamy A, Velumani A. National seroprevalence of Toxoplasma gondii
in India. J Parasitol 2007;93:1520-1.
Elhence P, Agarwal P, Prasad KN, Chaudhary RK. Seroprevalence of Toxoplasma gondii
antibodies in North Indian blood donors: Implications for transfusion transmissible toxoplasmosis. Transfus Apher Sci 2010;43:37-40.
Sundar P, Mahadevan A, Jayshree RS, Subbakrishna DK, Shankar SK. Toxoplasma seroprevalence in healthy voluntary blood donors from Urban Karnataka. Indian J Med Res 2007;126:50-5.
] [Full text]
Moncada PA, Montoya JG. Toxoplasmosis in the fetus and newborn: An update on prevalence, diagnosis and treatment. Expert Rev Anti Infect Ther 2012;10:815-28.
Luft BJ, Remington JS. Toxoplasmic encephalitis in AIDS. Clin Infect Dis 1992;15:211-22.
Khurana S, Batra N. Toxoplasmosis in organ transplant recipients: Evaluation, implication, and prevention. Trop Parasitol 2016;6:123-8.
] [Full text]
Martino R, Maertens J, Bretagne S, Rovira M, Deconinck E, Ullmann AJ, et al
. Toxoplasmosis after hematopoietic stem cell transplantation. Clin Infect Dis 2000;31:1188-95.
Palmer BS. Meta-analysis of three case controlled studies and an ecological study into the link between cryptogenic epilepsy and chronic toxoplasmosis infection. Seizure 2007;16:657-63.
Torgerson PR, Mastroiacovo P. The global burden of congenital toxoplasmosis: A systematic review. Bull World Health Organ 2013;91:501-8.
Singh S, Munawwar A, Rao S, Mehta S, Hazarika NK. Serologic prevalence of Toxoplasma gondii
in Indian women of child bearing age and effects of social and environmental factors. PLoS Negl Trop Dis 2014;8:e2737.
Maenz M, Schlüter D, Liesenfeld O, Schares G, Gross U, Pleyer U. Ocular toxoplasmosis past, present and new aspects of an old disease. Prog Retin Eye Res 2014;39:77-106.
Wilking H, Thamm M, Stark K, Aebischer T, Seeber F. Prevalence, incidence estimations, and risk factors of Toxoplasma gondii
infection in Germany: A representative, cross-sectional, serological study. Sci Rep 2016;6:22551.
Robert-Gangneux F, Dardé ML. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 2012;25:264-96.
Nowakowska D, Stray-Pedersen B, Spiewak E, Sobala W, Małafiej E, Wilczyński J. Prevalence and estimated incidence of toxoplasma infection among pregnant women in Poland: A decreasing trend in the younger population. Clin Microbiol Infect 2006;12:913-7.
Rudin C, Hirsch HH, Spaelti R, Schaedelin S, Klimkait T. Decline of seroprevalence and Incidence of congenital toxoplasmosis despite changing prevention policy-three decades of cord-blood screening in North-western Switzerland. Pediatr Infect Dis J 2018;37:1087-92.
Mizani A, Alipour A, Sharif M, Sarvi S, Amouei A, Shokri A, et al
. Toxoplasmosis seroprevalence in Iranian women and risk factors of the disease: A systematic review and meta-analysis. Trop Med Health 2017;45:7.
Gargaté MJ, Ferreira I, Vilares A, Martins S, Cardoso C, Silva S, et al
. Toxoplasma gondii
seroprevalence in the Portuguese population: Comparison of three cross-sectional studies spanning three decades. BMJ Open 2016;6:e011648.
Villard O, Cimon B, L'Ollivier C, Fricker-Hidalgo H, Godineau N, Houze S, et al
. Serological diagnosis of Toxoplasma gondii
infection: Recommendations from the French National Reference Center for Toxoplasmosis. Diagn Microbiol Infect Dis 2016;84:22-33.
Papadia M, Aldigeri R, Herbort CP. The role of serology in active ocular toxoplasmosis. Int Ophthalmol 2011;31:461-5.
Gontijo da Silva M, Clare Vinaud M, de Castro AM. Prevalence of toxoplasmosis in pregnant women and vertical transmission of Toxoplasma gondii
in patients from basic units of health from Gurupi, Tocantins, Brazil, from 2012 to 2014. PLoS One 2015;10:e0141700.
Sarkar MD, Anuradha B, Sharma N, Roy RN. Seropositivity of toxoplasmosis in antenatal women with bad obstetric history in a tertiary-care hospital of Andhra Pradesh, India. J Health Popul Nutr 2012;30:87-92.
O'Bryan TA, Okulicz JF, Bradley WP, Ganesan A, Merritt SE, Agan BK. Toxoplasma gondii
seroprevalence: 30-year trend in an HIV-infected US military cohort. Diagn Microbiol Infect Dis 2016;84:34-5.
[Figure 1], [Figure 2]
[Table 1], [Table 2]