To the authors' knowledge, this is the first study reporting the seroprevalence of anti-T. gondii in homeless persons, as well the first concomitant anti-T. gondii and anti-HIV seroprevalence associated with risk factors.
The seroprevalence of anti- T. gondii antibodies herein (35.8%) was higher than other vulnerable populations, such as aborigines (20.6%) and pregnant refugee and borderline migrant women (31.7%) but similar to incarcerated populations (37.6%) [11–13]. In Brazil, the anti-T. gondii seroprevalence herein was higher than the general population of the northeastern region, with 14/65 (21.5%) seropositive urban students, but lower than the central-western region, with 113/116 (97.4%) farmers from a single dairy cattle farm with domestic cats and potentially contaminated environment [51, 52]. Interestingly, the seroprevalence of anti-T. gondii antibodies in the present study was lower than other Brazilian neglected populations, such as 131/231 (56.7%) persons of riverside communities in the northern and 119/148 (80.4%) indigenous persons in the central-western region [53, 54]. In São Paulo, similar results were found, with 110/339 (32.4%) seropositive children from a low-socioeconomic community [55]. Not surprisingly, a previous study has shown an association between high seropositivity for T. gondii and socioeconomic vulnerability in southern Brazil, with 526/715 (73.57%) seropositive individuals, particularly in low-income families [56].
Although low education and socioeconomic status have been associated with increased risk of T. gondii infection in different Brazilian studies [57–59], no statistical association with T. gondii infection was previously found regarding educational background and income, probably due to the broadly variable classification of and the low population homogeneity [60, 61]. Similarly, no association was found in either education or income, likely associated to the impact of the vulnerable living style, with mostly drug addicts with poor eating habits.
Since the low socioeconomic status may be associated to malnutrition and might impair the host defense against protozoan infection, the relatively low seroprevalence of anti- T. gondii antibodies in homeless herein may be consequence of mainly consumption of ready-to-eat foods, as already indicated by previous studies on homelessness and food preparation facilities, which have reported dependence on charity meals such as pre-prepared foods, processed foods or popular snacks [62–65]. Not surprisingly, pre-processed ready-to-eat and meat-based foods have been shown to inactivate T. gondii cysts [66].
In addition, healthier and more expensive items such as meat, fish, vegetables, and fruits have been less often consumed by homeless [62, 65, 67, 68], which may be a contributing factor to the low T. gondii seroprevalence found in this study. Hence, it is reasonable to speculate that the beneficial shelters, hostels, and meal services may have offered protection to the homeless population [65, 69] but not as nutritional good food habits when compared to the general population. Although no homeless persons has been diagnosed with either anemia by packed cell volume (PCV) or hypoproteinemia by refractometry, such tests may not have enough sensitivity to detect chronic alimentary deficiencies, which should be further investigated.
A previous study with pregnant women has shown high seroprevalence of specific anti-T. gondii antibodies (68.4%; 333/487) and vertical transmission associated with social vulnerability in central Brazil [70]. In the present study, despite negative for both IgG and IgM anti- T. gondii antibodies, the two pregnant women sampled, fortunately, gave birth to clinically healthy babies. T. gondii infection during pregnancy has been a significant problem, especially during the first months, and may result in spontaneous abortion, fetal and/or neonatal death or several congenital disabilities such as hydrocephalus, central nervous system disorders, and chorioretinitis [71, 72]. In the second and third trimester, newborns have usually been asymptomatic, with symptoms appearing late in childhood or early in adulthood, and may sporadically cause visual impairment [71, 73, 74]. In addition, congenital toxoplasmosis may also be associated with reactivation of the chronical maternal infection, particularly in HIV-infected and immunosuppressed women [75]. As 7/8 (87.5%) women herein were within reproductive age and presented negative serology for T. gondii, the homeless may be highly unprotected to infection during pregnancy.
Although the present study has shown no association between T. gondii infection and pet ownership, including stray cat owners, corroborating with previous studies in rural and other vulnerable populations of southern Brazil [56, 60], only 6/120 (0.5%) homeless persons owned a total of 11 cats. Outdoor lifestyle of stray cats may include hunting of birds and rodents, leading to raw meat dietary habits and increased risk of T. gondii ingestion [76]. Nonetheless, human toxoplasmosis outbreaks may be attributed to exposure to infected cats, which may indicate an important role of cat oocyst excretion on infection spreading [77, 78], and homeless might be daily overexposed to environmental contamination. However, as mentioned above, homeless dietary habits of high intake of processed foods and low fresh meat, fish, vegetables and fruits may have led to lower T. gondii exposure.
Despite the HIV seroprevalence of 2/120 (1.7%) in homeless persons was above the estimated prevalence of 0.4% for the general Brazilian population and lower than a recent study with 69/1,402 (4.9%) seropositive homeless, was similar to other studies that showed 6/481 (1.2%) and 6/330 (1.8%) prevalence in homeless persons in Brazil, 181/10657 (1.7%) in Iran and 6/329 (1.8%) homeless women in the USA and within worldwide HIV prevalence in homeless persons ranging from 0.6% in Los Angeles to 23.5% in South Africa [24, 25, 79–81].
Although T. gondii and HIV co-infection has been widely studied due to the consequences that may occur in pregnant women and immunocompromised persons, no study to date has focused on the homeless population. Despite previous studies have shown a high prevalence of such coinfection, with 35.8% worldwide in a meta-analysis study and up to 88.4% of individuals coinfected in Ethiopia [39, 40], analysis of associated risk factor was not possible herein due to low HIV positive rate.
Despite frequent alcohol and drug use of homeless persons have been already observed in Brazil and worldwide [20, 26, 82, 83] and with higher infection risk to HIV and T. gondii in general population studies [41, 84, 85], there was no statistical association observed in the present study. Although one HIV-positive homeless person herein with multiple infections also declared himself as alcohol, marijuana, and skunk cannabis user, the other HIV-positive homeless persons denied alcohol and drug use.
Body lice (Pediculus humanus humanus) has been recently considered as a reemerging problem among homeless populations in France, Italy, USA, Colombia, and Brazil [48, 86–89]. Even though body lice presence suggests social vulnerability and 17/120 (14.2%) of the homeless herein were infested with lice, no statistically risk of T. gondii exposure was found.
As limitations of the present study, the most recent report of HIV homeless prevalence in São Paulo of 4.9% [20] was used for calculation of minimum sampling size since no T. gondii was available at the time. However, our HIV outcome prevalence of 1.7% was 2.9-fold lower than this study used as the basis for calculation but very similar to a previous 1.8% found in the homeless of São Paulo [25]. In addition, questionnaires to assess homeless information may be problematic, particularly regarding food intake and dietary habits, once such a population has often shown a chaotic lifestyle and a high prevalence of drug use and mental health disorders [65].