Knowledge and Practices of Toxoplasmosis among Clinical Laboratory Professionals: A Cross-Sectional Study in Durango, Mexico

Background: The aim of this study was to determine the level of knowledge and practices about toxoplasmosis in a sample of clinical laboratory professionals in Mexico. Methods: 192 clinical laboratory professionals were surveyed. They were asked about (1) Toxoplasma gondii; (2) clinical manifestations, diagnosis, treatment, and epidemiology of toxoplasmosis; and (3) their practices with respect to toxoplasmosis. Results: The range of animals infected by T. gondii was known by 44.8% of participants. Clinical aspects of toxoplasmosis were known by up to 44.3% of subjects. Correct answers about the interpretation of serological markers of T. gondii infection were provided by up to 32.8% of participants. A minority (32.2%) of participants knew about a high number of false positive results of anti-T. gondii IgM antibody tests. Most participants (90.1%) did not know what the anti-T. gondii IgG avidity test was. Up to 55.7% of participants provided incorrect answers about the interpretation of serology tests for the treatment of pregnant women. Common routes of T. gondii infection were known by <15% of participants. Most (84.4%) participants had not performed tests for detection T. gondii infection. Conclusions: Results indicate incomplete knowledge of T. gondii infection and toxoplasmosis and a limited practice of laboratory tests among the professionals surveyed.


Introduction
The parasite Toxoplasma gondii (T. gondii) causes infections in humans and animals, and is highly prevalent throughout the world [1][2][3]. Nearly one-third of the human population has been infected with T. gondii [4]. Transmission of T. gondii occurs mainly by ingestion of meat containing tissue cysts or by consumption of water or food containing oocysts shed by cats [5]. The definitive host of T. gondii are felids [6], and this intracellular parasite infects a wide range of warm-blooded intermediate hosts [7]. Other routes of T. gondii infections include congenital [8], blood transfusion [9], or organ transplant [10]. Most infections with T. gondii are asymptomatic [11]. However, toxoplasmosis, the disease caused by T. gondii, is characterized by retinochoroiditis [12] or cervical lymphadenopathy [5]. In immunocompromised individuals, a reactivation of a latent T. gondii infection may lead to life-threatening encephalitis [5]. Primary T. gondii infection in pregnant women can cause miscarriage [13] or fetal damage [14]. Routine tests for the diagnosis of T. gondii infection are based on serology [15]. Enzyme-linked immunosorbent assays and enzyme-linked fluorescent assays are tests currently used for detection of anti-T. gondii IgG and IgM antibodies in humans [16]. T. gondii commercial IgM diagnostic test kits can yield a number of false-positive results [17,18]. Anti-T. gondii IgM antibodies can persist for several years and a chronic T. gondii infection can be erroneously classified as an acute infection if diagnosis is based on IgM serology only [18]. Avidity tests of specific anti-T. gondii IgG antibodies are an important tool for discrimination of recent and past infections, especially in pregnant women [19,20]. Other serological tests for the diagnosis of T. gondii infection, i.e., Western blot [21] and indirect immunofluorescence test [22], are used less frequently. Confirmation of the presence of anti-T. gondii antibodies has been performed by Western blot [23]. Polymerase-chain-reaction-based molecular techniques are also useful for the diagnosis of T. gondii infection [24].
There is currently no report about knowledge and practices of toxoplasmosis among laboratory workers. Physicians, chemists, biologists, and technicians are professionals usually working in clinical laboratories, and it is important to know the knowledge and practices about toxoplasmosis because this would help to diagnose T. gondii infection by performing specific T. gondii laboratory tests. This information is useful for the design of optimal strategies for education and health care. The aim of the present study was to determine the level of knowledge and practices of toxoplasmosis in a sample of laboratory professionals in Mexico.

Study Design and Population Studied
We performed a cross-sectional study of laboratory professionals attending the XVI National Congress of Clinical Chemistry and Laboratory Medicine held in 2016 in Durango City, Mexico. Inclusion criteria for enrollment were as follows: (1) physicians, chemists, biologists, and technicians working in clinical laboratories in Mexico; (2) those who voluntarily participated in the survey. Age, gender, type of area in which the professionals work (urban, suburban, or rural), or whether they work for private and/or public organizations were not restrictive criteria for enrollment. In total, 192 participants were surveyed. General characteristics of the study population are shown in Table 1.

Questionnaire
A questionnaire was designed to record general data of participants, as well as their knowledge and practices of toxoplasmosis. The questionnaire was anonymous and self-administered. Most questions of the questionnaire were multiple-choice questions, and some were open-ended questions. Items of general data are shown in Table 1. Items to assess the knowledge and practices of toxoplasmosis included questions about the infectious agent, clinical aspects of the infection (Table 2), questions about the laboratory diagnosis and treatment (Table 3), questions about the epidemiology of T. gondii infection (Table 4), and questions about the practices with respect to toxoplasmosis at their workplace ( Table 5).

Statistical Analysis
The statistical analysis was performed with the aid of the software Epi Info 7 (Centers for Disease Control and Prevention, Atlanta, GA, USA), and SPSS 15.0 (SPSS Inc. Chicago, IL, USA). Descriptive statistics (percentages) were used to summarize and describe the data. Correlation of variables was analyzed by the Pearson's chi-square test and Fisher´s exact test (when values were small). A p-value < 0.05 was considered statistically significant.

General Data of Participants
Most participants were female (73.4%), worked in urban areas (93.8%), worked in public laboratories (93.8%), worked in Durango State (56.8%), were chemists or biologists (60.4%), were younger than 30 years old, and had less than 10 years of seniority in terms of their work (58.9%) ( Table 1).

Knowledge of the Parasite and Clinical Aspects of Toxoplasmosis
Results about the knowledge and clinical characteristics of toxoplasmosis are shown in Table 2. Most participants answered correctly that T. gondii is a parasite (89.6%), widely distributed in the world (76.6%), and having felids as definitive hosts (83.8%). In contrast, less than half of the participants knew that T. gondii infects a wide range of animals and birds (44.8%). Encephalitis was the most (44.3%) frequently recognized clinical characteristic of toxoplasmosis.

Knowledge of the Diagnosis and Treatment of Toxoplasmosis
Results about the knowledge of diagnosis and treatment of toxoplasmosis are shown in Table 3. Concerning interpretation of T. gondii serology, 32.8% of participants answered correctly that a positive test for IgG with a negative test for IgM means a chronic infection. The question that the routine test for detection of anti-T. gondii IgM antibodies in serum yields a high number of false positive results was answered correctly by 32.2% of participants. The great majority of participants (90.1%) did not know what an anti-T. gondii IgG avidity tests was, and 90.6% did not know what an avidity test was used for. Knowledge of avidity tests was similar among participants regardless of their type of training (p = 0.83) or the amount of seniority they had (p = 0.29). No other tests for the diagnosis of T. gondii infection were known by 83.9% of participants. Of those who knew about other tests for the diagnosis of T. gondii infection, 45.2% provided a good answer about T. gondii tests. Most (55.7%) participants answered that the demonstration of anti-Toxoplasma IgG and IgM antibodies in the serum of a pregnant woman was enough reason to provide treatment, and 42.2% of participants answered that the demonstration of anti-Toxoplasma IgM antibodies without IgG in the serum of a pregnant woman was enough reason to provide treatment.

Knowledge of the Epidemiology of Toxoplasmosis
Results about the knowledge of the epidemiology of toxoplasmosis are shown in Table 4. Half (50%) of the participants answered that contact with cats was a route of T. gondii infection, whereas ingestion of water, raw or undercooked meat, and unwashed fruits or vegetables were choices answered by less than 15% of participants. With respect to the world prevalence of T. gondii infection, 19.8% of participants answered that up to one-third of the population was infected by T. gondii.

Practices about Toxoplasmosis
Results about the practices of toxoplasmosis are shown in Table 5. The great majority (84.4%) of participants had not performed tests for detection of infection with T. gondii at their workplace. Concerning the question of which tests were used in their laboratory for detection of infection with T. gondii in pregnant women, 57.3% answered that anti-T. gondii IgG and IgM tests. With respect to the performance of confirmatory tests for T. gondii infection, 92.7% answered no performance. However, of 14 participants who answered that confirmatory tests were performed in their workplace, only 4 (28.6%) provided a good answer about the type of confirmatory tests used. Most (91.7%) participants answered that no molecular tests for T. gondii infection were performed in their workplace. Of 16 participants who answered that molecular tests were performed in their workplace, 9 (56.3%) provided a good answer about the type of molecular tests used.

Discussion
Studies about the knowledge and practices of toxoplasmosis among health care professionals are scanty. We are not aware of any study about the knowledge and practices of toxoplasmosis among laboratory professionals. Therefore, this study was aimed to determine the knowledge and practices about toxoplasmosis among a sample of laboratory professionals attending a national congress of clinical chemistry and laboratory medicine in Durango City, Mexico. Results suggest that most laboratory professionals had good knowledge of the general characteristics of T. gondii since 89.6% of participants knew that T. gondii is a parasite, 76.6% knew that it is distributed worldwide, and 83.8% knew that felids are the definitive hosts of T. gondii. However, less than half (44.8%) of participants knew that T. gondii infects a wide range of animals and birds. With respect to clinical characteristics of toxoplasmosis, only one question, including well recognized clinical features of toxoplasmosis, was asked. Less than 30% of participants knew that lymphadenopathy and ocular disease occurs in toxoplasmosis, whereas 44.3% of participants knew that encephalitis occurs in toxoplasmosis. However, encephalitis occurs mostly in immunocompromised patients [5] and therefore, it is not a common clinical manifestation of toxoplasmosis. Results thus suggest a suboptimal knowledge of basic clinical characteristics of toxoplasmosis among our study population. Concerning questions of the knowledge of the interpretation of laboratory results for the diagnosis and treatment of toxoplasmosis, a limited number of participants answered correctly. The only correct answer about the interpretation of laboratory tests, which was that a positive test for IgG with a negative test for IgM anti-T. gondii indicates a chronic infection, was given by 32.8% of participants. The statement that the routine test for detection of anti-Toxoplasma IgM antibodies in serum yields a high number of false positive results was correctly chosen by 32.3% of participants. Remarkably, only 9.9% of participants knew the anti-T. gondii IgG avidity test, and only 2.6% of those who knew it had knowledge of what it was used for. The vast majority (83.9%) did not know about tests other than the IgG and IgM tests for the diagnosis of T. gondii infection. With respect to questions about the interpretation of laboratory tests to justify the treatment, only 18.8% of participants correctly answered that it was false that the demonstration of anti-T. gondii IgG and IgM antibodies in the serum of a pregnant woman is enough reason to provide treatment. Anti-T. gondii IgM antibodies can be present for years and do not necessarily indicate acute infection in pregnant women [18]. Similarly, only 29.2% of participants knew that the demonstration of anti-T. gondii IgM antibodies without IgG in the serum of a pregnant woman is not enough reason to provide treatment. All pregnant women with a positive anti-T. gondii IgM test should be further examined with the anti-T. gondii IgG avidity test to discriminate between acute and past infections [19,20]. Only women with low anti-T. gondii IgG avidity should be considered for treatment [19,20]. Poor knowledge of the avidity test found in the present study has also been reported with respect to physicians attending pregnant women in Mexico [25] and the USA [26].
With respect to knowledge of the epidemiology of toxoplasmosis, many participants did not correctly answer questions about important routes of infection with T. gondii. T. gondii infection can be acquired by ingestion of water or food contaminated with oocysts shed by cats and by the consumption of raw or undercooked meat containing tissue cysts [5]. In fact, T. gondii infection has been associated with consumption of unwashed raw vegetables [27], fruit [28], and untreated water [29] in Mexico.
The most frequent answer regarding the transmission of T. gondii given by the participants was contact with cats. The factor presence of cats at home has been associated with T. gondii infection in Durango, Mexico [29][30][31][32]. However, direct contact with cats is not thought to be a primary risk for human infection [33]. It is estimated that nearly one-third of the world's population is infected with T. gondii [4]. In this study, only 19.8% of participants answered correctly that up to one-third of the population is infected with T. gondii. The results thus indicate that the laboratory professionals surveyed had incomplete knowledge of the epidemiology of T. gondii infection.
With respect to the practices of toxoplasmosis, most participants stated that no laboratory tests for detection of T. gondii infection are performed in their workplace. This finding may reflect the scanty use of tests for the diagnosis of T. gondii infection in clinical laboratories in Mexico. The screening of T. gondii exposure is based on the determination of anti-T. gondii IgG and IgM antibodies [15,16]. However, in the present study, only 57.3% of participants informed that these infection markers were performed to detect T. gondii infection in pregnant women in their laboratories. The use of serology tests for the confirmation of T. gondii infection or molecular tests to detect T. gondii DNA is very rare in Mexico as reported by the great majority of participants surveyed. Results thus indicate that laboratory professionals surveyed had a limited practice about clinical laboratory tests for the diagnosis of T. gondii infection.
Our study has some limitations. We studied only attendees of a national congress and most of them were working in one state (Durango) of Mexico. These results thus cannot be extrapolated to laboratory professionals in the whole country.

Conclusions
This is the first study on knowledge and practices of toxoplasmosis among laboratory professionals. Results indicate incomplete knowledge of T. gondii infection and toxoplasmosis including interpretation of laboratory tests, clinical features, epidemiology and treatment, and a limited practice of laboratory tests among the professionals surveyed. These results can be useful for the design of strategies leading to optimal education about clinical laboratory tests for the diagnosis of T. gondii infection.