³ Department of Zoology, Charles University, Vinièná 7, Prague 128 44, Czech Republic

Table 2.

Correlations between personality factors and the duration of chronic toxoplasmosis. The raw personality data were used as dependent variables and the age of the subjects as a covariate.

using the age of a person as a covariate. The results are summarised in Table 3. From 16 factors studied, only G (superego strength) systematically changed (decreased) during the 13 years following Toxoplasma gondii infection (R* = 0.02, t(162)=2.14, p=0.017, one-tailed t test) (see Fig. 1). It was the same factor that was significantly lower (F(1, 221)=5.92, p=0.016) in Toxoplasma infected men in our first experimental set (Biologists). A statistically insignificant tendency also existed (R*=0.016, t(162)=-1.88, p=0.062, a two-tailed t test) for the decrease of B (intelligence). This decrease became significant (p=0.014) when the data of eleven (11) persons diagnosed with toxoplasmosis before the age of six (possibly congenital toxoplasmosis) were also included into analysis.

Correlation between the length of infection and superego strength.The abscissa shows the residuals of regression between age and the raw personality factor G, the ordinate shows the time (in months) from the first positive test for acute toxoplasmosis.

4. DISCUSSION

Our results demonstrated the existence of a correlation between anti-toxoplasma immunity (monitored by IDTH) and certain personality factors in men and women. The existence of a correlation between the extent of personality factor shift and the duration of toxoplasmosis suggests that toxoplasmosis induces a shift in human personality, rather than the personality factor shift influences the probability of being infected with Toxoplasma gondii.

Positive reaction in IDHT indicates the existence of cellular immunity. Cellular immunity against T. gondii may require months to develop. It lasts many years, possibly for the rest of the host's life. These two facts make IDHT superior in comparison with any serological test for diagnosis of latent infection (Remington & Krahenbuhl, 1982). It is not known, however, if cellular immunity necessarily indicates latent toxoplasmosis, e.g. the presence of live parasites in cysts in nervous and muscular tissues of the immune subject. Experience with AIDS patients suggests that the frequency of latent toxoplasmosis in human population may be identical with the frequency of Toxoplasma-immune subjects (Roberts, Murrell & Marks, 1994). Also our results on correlation of the shift of factor G (decrease of the superego strength) with the duration of toxoplasmosis indicate that the parasites in the cysts may be alive and biologically active for many years after infection. However, it must still be clarified whether the process of the personality factor-shift is directed by the encysted Toxoplasma bradyzoites, or whether it is only triggered by the acute stage of the infection.

The results from the MANCOVA suggest that personality factors G, L, and possibly O, A, and Q3 might be shifted in Toxoplasma-infected men, and factors A, L, and possibly N and Q3 in Toxoplasma infected women. On the other hand, in the discriminant analysis (and so in Logistic regression, results not shown) another group of factors (L, G, F, Q2 for men and A, L, Q2 for women) proved to be most useful for the identification of Toxoplasma-infected subjects. This discrepancy can be explained by differences in the mathematical background of these two methods. Discriminant analysis includes a stepwise covariance analysis. In every step, F-to-enter values are affected by the variables already present in the classification function. When a strong correlation exists between two variables (e.g. factor G and Q3) only the one with a higher F value might enter the classification function. On the other hand, when low or no correlation exists among variables, all might enter the function despite their relatively low F values in the step zero of discriminant analysis (or in MANCOVA).

In the men's subset the factors G (low superego strength), L (protension), F (desurgency), and Q2 (group dependency) are positively influenced by toxoplasmosis (as indicated by discriminant analysis). In the women's subset the factors A (afectothymia), L (alaxia) and Q2 (self sufficiency) are more pronounced in the Toxoplasma-infected subjects. The nature of involved factors (see Table 1) as well as the fact, that the same factors are often shifted in the opposite direction in the men and women subsets, make the biological or psychological interpretation of the toxoplasmosis-induced changes of the personality profiles very difficult. It has been demonstrated that T. gondii-infected animals (rodents) are less anxious (Hutchison et al. 1980a), less neophobic (Webster et al. 1994), more active (Hutchison, 1980a; Webster et al.1994) and aggressive (Arnott et al. 1990) than the controls. It can be speculated whether the low superego strength, i.e. tendencies to disregard the societal rules, may be determined or influenced by lack of fear of punishment and/or by an aggression in men and by another factor in the women. Analogically A (afectothymia), i.e. warmheartedness, outgoingness, easygoingness may be controlled or influenced by lack of fear in the women, and by other factor(s) in men, depending on the difference between men's and women's social roles. The existence of gender-specific differences in the composition of certain personality factors is suggested by the difference in the structures of covariance matrices of Cattell's personality factors for men and women (results not shown).

It must be also stressed that the character of toxoplasmosis induced changes in the behaviour of humans and rodents may be dramatically different even if they are induced by the same mechanism. In the rodent system the ability to decrease neophobia and anxiety and to increase the activity of its intermediate host is highly adaptive for Toxoplasma. Such manipulation can positively influence the probability of transmission of T.gondii into the definitive host (felid) by carnivorism. In modern man such parasite activity is non-productive so the parasite is expected to be better adapted for manipulation of rodent behaviour. The changes in human behaviour (monitored by the changes in the personality profiles in our study) probably only indirectly reflect some activity of T. gondii, possibly the synthesis or induction of synthesis of dopamine (Stibbs, 1985) or of other biologically active substances (Silverman & Varela, 1958) in the host brain tissue.

The data from fifteen patients infected within the past six months were excluded from our correlation analysis. Acute toxoplasmosis often shows a symptomatic period with fever, general malaise, headache, dizziness, sore throat, coughing. Accompanying psychopathological features are very common and frequently include depression, apathy and anxiety, often anxiety spells, and paraesthesia (Ladee, Scholten & Posthumus Meyes, 1966 ). Many of these neurological and psychopathological symptoms may be toxoplasmosis-nonspecific. In our study a dramatic shift in personality profiles was detected in a group of fifteen patients recently infected by T. gondii as well as in a group of forty-three patients with toxoplasmosis-like symptoms but with negative results in toxoplasmosis immunological tests (complement fixing reaction, ELISA IgM, ELISA IgA, indirect fluorescent antibody test) (data not shown). Similar effects of acute toxoplasmosis have already been reported by others (Höschl & Balon, 1980).

The data from eleven men diagnosed with toxoplasmosis before age six and therefore suspected of having a congenital form of toxoplasmosis were also excluded from the analysis. The neurological manifestation of congenital toxoplasmosis due to meningoencephalitis is relatively frequent, and the sequelae includes psychomotor and mental retardation (Koppe & Rothova, 1989). We suppose that the observed correlation between the decrease of factor B (intelligence) and the length of latent toxoplasmosis might be caused by the presence of unrecognised cases of congenital toxoplasmosis in our acquired toxoplasmosis-experimental set (mainly within the long-duration toxoplasmosis subset).

The influence of severe forms of acute toxoplasmosis on human personality has been reported by many clinicians (Burkinshaw, Kirman & Sorsby, 1953; Minto & Roberts, 1959; Ladee et al. 1966; Freytag & Haas, 1979). In literature, attention is frequently focused on psychoses with schizophrenic features that accompany latent toxoplasmosis or toxoplasmosis acquired in childhood or early adult life (for review see Ladee et al. 1966). Numerous studies have also shown an excess of Toxoplasma-infected subjects among patients in mental hospitals, (Robertson, 1966; Thalhammer, 1962; Garcia, 1979; Garrido et al. 1978). Typically, however, the effects of acquired toxoplasmosis on immunocompetent subjects are mild; only a negligible fraction of infected subjects ever learn that they are parasitized. Latent toxoplasmosis acquired in adult life is usually considered asymptomatic (Remington, 1974). In this respect the existence of easily detected differences between Toxoplasma-infected and Toxoplasma-free biologists was unexpected. One can only speculate, whether these activities of the parasite are connected with an attempt (in modern humans a nonproductive one) of the parasite to manipulate the host behaviour, or are only byproducts of a nonspecific decline in the quality of host life. Infected subjects might theoretically suffer more frequent or more severe diseases because of an interference by the parasite with their immune system (Krahenbuhl & Remington, 1982; Remington & Krahenbuhl, 1982). Such effects of toxoplasmosis, however, have never been reported.

This research was supported by the Czech Biological Foundation and grant GUK95. We thank A. Exnerova for her help with psychological questionnaires and K. Zvara for help with the statistical analysis. We also thank our colleagues who participated in the experiments.

REFERENCES

ARNOTT, M. A., CASSELLA, J. P., AITKEN, P. P. & HAY, J. (1990). Social interactions of mice with congenital Toxoplasma infection. Annals of Tropical Medicine and Parasitology 84, 149-56.

BARNARD, C.J. & BEHNKE, J.M. (eds.) (1990). Parasitism and Host Behaviour. New York, Philadelphia, London: Taylor and Francis.

BOUŠKA, V., DELANO, J. W., MASLOWSKÁ, H. & ŘANDA, Z. (1990). Discriminant analysis of the moldavite data set. Acta Universitatis Carolinae-Geologica 3, 243-58.

BURKINSHAW, J., KIRMAN, B. H. & SORSBY, A. (1953). Toxoplasmosis in relation to mental deficiency. British Medical Journal 702, 1-6.

CATTELL, R.B. (1970). Handbook for the sixteen personality factors questionnaire (16PF). Champaign: Institute for Personality and Ability Testing.

DESMONTS, G. & COUVREUR, J. (1974). Congenital toxoplasmosis. A prospective study of 378 pregnancies. New England Journal of Medicine 290, 1110-16.

FELDMAN, H. A. (1954). Laboratory methods in current use for the study of toxoplasmosis. Advances in Ophthalmology Vol. III, (ed. E. B. Streiff), Lausanne Bibliotheca Ophthalmologica Fascicles 39, 1-11.

FLEGR, J. & HRDY, I. (1994). Influence of chronic toxoplasmosis on some human personality factors. Folia Parasitologica 41, 122-26.

FREYTAG, H. W. & HAAS, H. (1979). Zur Psychopathologie der erworbener Toxoplasmose. Nervenarzt 50, 128-31.

GARCIA, G. D. (1979). Toxoplasmosis y enfermedades mentales. (Toxoplasmosis and mental diseases) Revista Cubana de medicica tropicales 31, 127-31.

GARRIDO, J.A., BOVEDA, M. I. C. & DEBECERRA, J. O. (1978). Estudio de la toxoplasmosis en un medio hospitalario psiquiatrico. Consecuencias clinicas y epidemiologicas (Studies on toxoplasmosis in the mental hospitals. Clinical and epidemiological aspects.) Diagnostico biologico XXVII, 267-88.

HAY, J., HUTCHISON, W. M., AITKEN, P. P. & GRAHAM, D. I. (1983). The effect of congenital and adult-acquired Toxoplasma infections on activity and responsiveness to novel stimulation in mice. Annals of Tropical Medicine and Parasitology 77, 483-95.

HAY, J., AITKEN, P. P. & AMOTT, M. A. (1985). The influence of congenital toxoplasma infection on spontaneous running activity of mice. Zeitschrift für Parasitenkunde 71, 459-62.

HÖSCHL, C. & BALON, R. (1980). Výsledky psychiatrického vyšetřování nemocných toxoplasmózou. (Results of psychiatric investigation of patients with toxoplasmosis). Časopis Lékaru českych 119, 366-68.

HUTCHISON, W. M., BRADLEY, M., CHEYNE, W. M., WELLS, B. W. P. & HAY, J. (1980 b). Behavioural abnormalities in Toxoplasma-infected mice. Annals of Tropical Medicine and Parasitology 74, 337-45.

KOPPE, J. G. & ROTHOVA, A. (1989). Congenital toxoplasmosis. A long-term follow-up of 20 years. International Ophthalmology 13, 387-90.

KRAHENBUHL, J. L. & REMINGTON, J. S. (1982). The immunology of Toxoplasma and toxoplasmosis. In Immunology of Human Infections, Part II A.(eds. J. Mahmias. & J O'Reily ), New York: Plenum Publishing Corporation.

LADEE, G. A., SCHOLTEN, J. M. & POSTHUMUS MEYES, F. E. (1966). Diagnostic problems in psychiatry with regards to acquired toxoplasmosis. Psychiatria Neurologia, Neurochirurgia 69, 65-82.

MINTO, A. & ROBERTS, F.J. (1959). The psychiatric complications of toxoplasmosis. The Lancet 275, 1180-82.

POKORNÝ, J., FRUHBAUER, TOMÁŠKOVÁ, V., KRAJHANZLOVÁ, L., SÝKORA, J. & ZÁSTERA, M. (1990). Stanoveni antitoxoplasmickych protilatek IgM metodou ELISA. (Estimation of antitoxoplasmatic IgM antibidies with the ELISA method.) Èeskoslovenska Epidemiologie 39, 57-62.

REMINGTON, J.S. (1974). Toxoplasmosis in the adult. Bulletin of the New York Academy of Medicine 50, 211-27.

REMINGTON, J.S. & KRAHENBUHL, J.L. (1982). Immunology of Toxoplasma gondii. In Immunology of Human Infection Part II (eds Nahmias, A. J. & O'Reilly, J.), pp. 327-371. New York: Plenum Publishing Corporation.

ROBERTS, T., MURRELL, K. D. & MARKS, S. (1994). Economic losses caused by foodborne parasitic diseases. Parasitology Today 10, 419-23.

ROBERTSON J. S. (1966). Toxoplasmin sensitivity: subnormality and environment. Journal of Hygiene 64, 405-10.

SILVERMAN & B. VARELA, G. (1958). Toxoplasmosis, mental disease and LSD-25. Revista del Instituto de salubridat y enfermedades tropicales 18, 191-94.

STIBBS, H. H. (1983). Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Annals of Tropical Medicine and Parasitology 79, 153-57.

THALHAMMER, O. (1962). Congenital toxoplasmosis. The Lancet I 278, 23-24.

WARREN, J. & SABIN, A.B. (1942). The complement fixation reaction in toxoplasmic infection. Proceedings of the Society for experimental Biology and Medicine 51, 11-16.

WEBSTER, J. P. (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology 109, 583-89.

WEBSTER, J. P., BRUNTON, C.F.A. & MACDONALD, D. W. (1994). Effect of Toxoplasma gondii on neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology 109, 37-43.