Folia Parasitologica, 1999, 46: 22-28

 

Changes in the personality profile of young women with latent toxoplasmosis
 
 
 
 
 

Jaroslav Flegr and Jan Havlíček
 

Department of Parasitology, Faculty of Science, Charles University, Vini?ná 7, 128 44 Prague, Czech Republic
 
 
 

Running head: Induction of personality changes by toxoplasmosis
 

Key words: Toxoplasma gondii, behavior, Cattell's questionnaire, manipulation hypothesis, permutation test.
 
 
 

Author for correspondence:

Jaroslav Flegr, Department of Parasitology, Charles University, Vini?ná 7, Prague 128 44, Czech Republic

telephone +4202-21953289, fax 004202-299713, email: flegr@ beba.cesnet.cz
 

Abstract. Latent toxoplasmosis is the most widespread parasite infection in developed and developing countries. The prevalence of Toxoplasma gondii infection varies mostly between 20 B 80% in different territories. This form of toxoplasmosis is generally considered to be asymptomatic. Recently published results, however, suggest that the personality profiles of infected subjects differ from those of uninfected controls. These results, however, were obtained on nonstandard populations (biologists or former acute toxoplasmosis patients). Here we studied the personality profiles of 191 young women tested for anti-Toxoplasma immunity during gravidity. The results showed that the differences between Toxoplasma-negative and Toxoplasma-positive subjects exits also in this sample of healthy women. The subjects with latent toxoplasmosis had higher intelligence, lower guilt proneness, and possibly also higher ergic tension. The difference in several other factors (desurgency/surgency, alaxia/protension, naivete/shrewdness, and self sentiment integration) concerned changes in the variances, rather then the mean values of the factors.
 

One of the most widespread parasites in the Czech Republic is the protozoon Toxoplasma gondii. The longtime prevalence in normal population of this parasite is about 30%, while the prevalence in higher age categories and within some risk groups increases above 50% (Nemec et al. 1988, Sengbusch and Sengbusch 1978, Yamaoka and Konishi 1993). Four distinct forms of toxoplasmosis exist. The most serious form is the congenital toxoplasmosis which often leads to serious malformations including hydrocephaly, intra-cerebral calcification and microcephaly (Koppe and Rothova 1989). The second form is the acquired acute toxoplasmosis. It is characteristic by the presence of T. gondii tachyzoites in a blood and in other tissues of infected people and by a complex of clinical symptoms which varies from fever and headache to serious neurological and psychiatric malfunctions (Kramer 1966). In the most cases, however, the acute toxoplasmosis is only a mild disease which is often misdiagnosed as a common bacterial or viral infection. Infrequently the acute toxoplasmosis evolves into chronic disease in which the clinical symptoms as well as high titres of specific antibodies persist for many years. Mostly, all symptoms of acute diseases quickly fall away, the antibody titres decrease and the toxoplasmosis evolves into the latent form of the infection. During the latent toxoplasmosis the parasite survives in the dormant form of bradyzoites mostly in the neural and muscular tissue of the host. The latent toxoplasmosis probably last for the whole life of infected person (Remington and Krahenbuhl 1982) and it can turn into acute toxoplasmosis only after serious violence of integrity of immune systems (AIDS, treatment with immunosupressive drugs etc. (Heitman and Irizarry 1997, Mocsny 1992)).

Latent toxoplasmosis is considered to be asymptomatic. Most of the infected people never learn to have met T. gondii in the past and carry the dormant stages of the parasite for the rest of their life. Recently, however, significant differences in personality profiles of men and women with latent toxoplasmosis and normal controls were reported to exist (Flegr and Hrdý 1994, Flegr et al. 1996). Toxoplasma-positive subjects differ by mean value of some psychologic factors measured by 16 PF Cattell=s personality questionnaire. The differences in some of these factors increase with the duration of latent toxoplasmosis (Flegr et al. 1996). This suggests that the changes were induced by the toxoplasmosis rather than the personality factor shift influencing the probability of being infected with T. gondii. Under natural conditions the intermediate hosts of Toxoplasma are small rodents and the final host is a cat. Therefore, the changes in the human personality can be a product of manipulation activity of the parasite which is primarily aimed to increase the probability of transmission from intermediate to a definitive host by predation. Such manipulation activity of T. gondii was observed in many experimental systems (Hutchison et al. 1980, Webster et al. 1994, Berdoy et al. 1995, Hutchison et al. 1980, Webster 1994, Arnott et al. 1990). The mechanism of manipulation activity of Toxoplasma gondii is not known. However, it can probably include the synthesis (or induction of synthesis) of some neuromodulator (Stibbs 1985) or of other biologically active substance (Varela et al. 1956, Varela et al. 1957). In the aberrant host (man) such activity of the parasite is of course nonproductive. However, it can manifest its presence by nonspecific (from the point of view of a manipulation hypothesis) changes in human personality.

In the previous studies the personality changes were studied either on population of biologists or on subjects previously diagnosed for acute toxoplasmosis (Flegr and Hrdý 1994, Flegr et al. 1996). Neither of the experimental sets represents a typical population. Therefore, it is difficult to guess whether the obtained results can by generalized for normal population. Moreover, in both cases the subjects were informed that the aim of the research is to reveal possible influence of toxoplasmosis on human personality. Such information could influence the subject=s responses on the questionnaire (at least in the second study in which the subjects were aware to be infected be Toxoplasma gondii before the questionnaire testing).

The aim of the present study was to find out whether the differences in personality profiles can be detected also in a random sample of normal women tested for toxoplasmosis during pregnancies. For ethical reasons (a possible fear of young mothers of congenital toxoplasmosis) the women could not be informed that the research concerns the toxoplasmosis. The absence of a priori knowledge about the subject of the research helped to eliminate possible intentional or unintentional data distortion by the experimental subjects. The results showed that personality profiles of women with latent toxoplasmosis significantly differed from those of women without the infection. The character and the amount of these personality changes were similar to those observed in the previous studies.

MATERIAL AND METHODS

Experimental subjects. The experimental set (young women) consisted of 191 women 18-39 years old who were serologically tested for toxoplasmosis during pregnancy. Among these women 146 tested negative and 55 have the titers of anti-Toxoplasma antibodies between 1 : 8 and 1 : 64 which indicates latent toxoplasmosis. According to the levels of IgG and IgM antibodies no woman involved suffered acute toxoplasmosis. All subjects (824) received the personality questionnaire 6-7 month after the serological examination, mostly 2-5 months after the childbirth. In the cover letter they were only asked to voluntarily participate in an unspecified research project (to avoid a possible fear of young mothers of congenital toxoplasmosis). The return rate was approximately 23.2%.

Personality tests. Cattell's sixteen factor questionnaire (form A) (Cattell 1970) was used for characterization of personality profiles. This questionnaire is still widely used for personality studies in many countries, including the Czech Republic. It covers sixteen personality factors (Tab. 1). The main advantage of this traditional is that it contains
 

Table 1. List of sixteen personality factors monitored by Cattell's questionnaire. The names and characteristics in the left column are for persons with low values of the factor, those in the right column for persons with high values of the factor. The traits that increase in young women with latent toxoplasmosis are typed in bold.
SIZOTHYMIA	A	AFFECTOTHYMIA
reserved, detached, critical		warm-hearted, outgoing, easygoing
LOW INTELLIGENCE	B	HIGH INTELLIGENCE
EGO WEAKNESS	C	HIGH EGO STRENGTH
affected by feelings, emotionally less stable		stable, mature, faces reality, calm
SUBMISSIVENESS	E	DOMINANCE OR ASCENDANCE
obedient, mild, easily led, docile		aggressive, competitive, stubborn
DESURGENCY	F	SURGENCY
sober, taciturn, serious		enthusiastic, heedless, happy- go -lucky
LOW SUPEREGO STRENGTH	G	SUPEREGO STRENGTH, CHARACTER
disregards rules, expedient		conscientious, persistent, moralistic, staid
THRECTIA	H	PARMIA
shy, timid, restrained,		adventurous, "thick-skinned', socially
HARRIA	I	PREMSIA
tough-minded, rejects		tender-minded, sensitive,
ALAXIA	L	PROTENSION
trusting, accepting conditions, tolerant		suspecting, jealous, dogmatic
PRAXERNIA	M	AUTIA
practical, has "down to earth"		imaginative, bohemian,
NAIVETÉ	N	SHREWDNESS
forthright, unpretentious		astute, worldly, polished
UNTROUBLED ADEQUACY	O	GUILT PRONENESS
self-assured, placed, secured		apprehensive, self-reproaching, insecure
CONSERVATISM OF TEMPERAMENT	Q1	RADICALISM
conservative, respecting		experimenting, liberal, analytical,
GROUP DEPENDENCY	Q2	SELF-SUFFICIENCY
sociably group dependent, "joiner"		self-sufficient, resourceful, prefers own decisions
LOW SELF-SENTIMENT INTEGRATION	Q3	HIGH STRENGTH OF SELF SENTIMENT
uncontrolled, lax, follows own urges		controlled, exacting will power, socially precise
LOW ERGIC TENSION	Q4	HIGH ERGIC TENSION
relaxed, tranquil, torpid,		tense, frustrated, driven, overwrought,

 

only one hundred and eighty-seven (187) questions. Therefore, it can be completed by most subjects within forty minutes. All subjects obtained the questionnaire by mail and were asked to voluntarily participate in an unspecified research project.

Immunological tests for toxoplasmosis. The latent toxoplasmosis in pregnant women was diagnosed with complement-fixation test (CFT), (Warren and Sabin 1942), in the National

Diagnostic Laboratory for Toxoplasmosis, National Institute of Public Health, Prague, Czech Republic. The titre of anti-Toxoplasma antibodies in sera was measured in dilutions between 1 : 8 and 1 : 1024. All subjects with the titres from 1 : 8 to 1 : 64 were considered latent toxoplasmosis positive, the subject with titre lower then 1 : 8 latent toxoplasmosis negative. No subjects with titres equal or higher than 1 : 128 (the indication of recent acute toxoplasmosis) were involved in our study.

Statistical tests. The computation of standard residuals by linear regression (for elimination of the effect of age), the t-tests and the Levene tests were performed by the program package Statistica7. The program TREEPT (originally called PTPT, (Flegr and Záboj 1997)) was used for all permutation tests including the permutation tests with elimination of false negative cases. This freeware Windows program for various permutation tail probability tests is available on the address http://www.natur.cuni.cz/~flegr/programs. The rationale of the permutation test is described in the legend of the Table 3. Differences in variances of personality factors between Toxoplasma negative and positive subjects were tested by the same permutation tests, however, the absolute values of age-standardized factors instead of age-standardized factors were entered into the program. The rationale of this approach was based on our previous observation that for certain personality factors both minimal and maximal extremes were absent in Toxoplasma positive subjects.

RESULTS

We obtained the personality data from 136 Toxoplasma-negative and 55 Toxoplasma-positive women. Effect of the age was eliminated be computation of standard residual of linear regression between the age and raw personality factors. The effect of latent toxoplasmosis was tested by t-test and the Levene's test for the homogeneity of variances. The results (Tab. 2) suggest that no differences in mean values of Cattell=s factors exist between Toxoplasma-negative and Toxoplasma-positive women.
 
 

Table 2. Differences in 16 Cattells factors between Toxoplasma-positive and Toxoplasma-negative women. The factors are described in the Table 1.

 

 
 
 
 
 
 

 

The diagnosis of latent toxoplasmosis was performed by complement fixation test. This simple serological test is very useful for rapid screening for acute toxoplasmosis. However, it often provides false negative results for subjects with low titers of antibodies, for example for subjects with very old T. gondii infections. Therefore, our subset of Toxoplasma-negative women must be contaminated by an unknown percentage of Toxoplasma-positive women. Such women with old infections (and consequently with low levels of specific antibodies) are known to have the highest amount of the personality factor shift (Flegr and Hrdý 1994, Flegr et al. 1996). Therefore, their presence in the Toxoplasma-negative subsets can flatten out any possible difference between the two subsets. The effects of such kind of data contamination can be revealed and eliminated by a permutation test with data reassignment. For this kind of tests we used the program TREEPT which can perform permutation tests analogical to t-test or ANOVA with reassignment of a particular fraction of cases from one group to the other (in this case from the subset of Toxoplasma-negative women to the Toxoplasma-positive subset). The results of this analysis are shown in the Table 3.

Table 3. The differences between Toxoplasma-negative and Toxoplasma-positive women tested by permutation tail probability test with data reassignation. The differences in particular age-standardised personality factor was tested by two-sided permutation test. From zero to 60% of subjects with the highest (or lowest) values of a tested factor were relocated from the group of 136 Toxoplasma-negative women to the second group of 55 Toxoplasma positive women. Then, the difference of means of these two groups was calculated. In next 2999 steps the empirical values of analysed factors were arbitrary assigned into two groups of the sizes 136 and 55 cases, the same percentage as before of highest (or lowest) cases from the larger group was relocated to smaller group and the difference of the means of the two groups was calculated. Finally, all 3000 differences (including the one calculated from nonpermutated data) were sorted from highest to lowest. The percentage of differences higher or equal to that calculated on the basis of nonpermutated data was considered as the statistical significance (p), i.e. the probability of obtaining the same or higher difference of means of groups 136 and 55 subjects assigned into these groups randomly. The difference in data distribution within the group was tested by the same approach. In this case, however, the absolute values of age-standardised factors instead of standardised factors were entered into the test.
 
 
 

Means

Distributions

 

	p(0%)	p(5%)	p(10%)	p(15%)	p(20%)	p(30%)	p(60%)	p(5%)	p(10%)
A	0.90	0.46	0.44	0.42	0.44	0.50	0.53	0.39	0.41
B	0.12	0.05	0.03	0.03	0.02	0.03	0.04	0.84	0.72
C	0.33	0.81	0.18	0.79	0.80	0.82	0.89	0.26	0.21
E	0.75	0.37	0.39	0.42	0.42	0.41	0.54	0.31	0.32
F	0.92	0.53	0.50	0.59	0.65	0.73	0.81	0.08	0.09
G	0.97	0.46	0.47	0.45	0.46	0.44	0.36	0.81	0.80
H	0.72	0.36	0.32	0.31	0.28	0.30	0.37	0.61	0.61
I	0.50	0.72	0.28	0.64	0.63	0.57	0.56	0.74	0.74
L	0.28	0.16	0.18	0.19	0.23	0.33	0.55	0.04	0.05
M	0.61	0.64	0.30	0.58	0.56	0.55	0.44	0.84	0.84
N	0.98	0.56	0.60	0.61	0.61	0.64	0.74	0.06	0.09
O	0.06	0.02	0.02	0.03	0.03	0.05	0.09	0.32	0.28
Q1	0.26	0.09	0.09	0.09	0.09	0.09	0.17	0.43	0.41
Q2	0.64	0.68	0.29	0.63	0.63	0.66	0.63	0.51	0.44
Q3	0.93	0.47	0.49	0.55	0.58	0.68	0.74	0.01	0.01
Q4	0.20	0.10	0.09	0.07	0.07	0.07	0.09	0.67	0.68

 
 
 
 
 

The results of permutation tests showed that the Toxoplasma-positive women had higher factor B (intelligence), factor O (guilt proneness) and possibly also Q4 (high ergic tension) and Q1 (radicalism). The differences between Toxoplasma-negative and Toxoplasma-positive women in the factors L and Q3, and possibly also F and N demonstrated its existence by changes in the character of distribution, rather then changes in the mean values of the factors. The histograms of standardised factors (not shown) suggest, that the distribution of values of these factors in Toxoplasma-positive women have lower kurtosis and can be approximated by the rectangular while that of Toxoplasma-negative women by the normal distribution.
 
 
 

DISCUSSION Our results suggest that the personality profiles of women with latent toxoplasmosis differ in certain factors from those of women without toxoplasmosis. Toxoplasma-positive women have higher intelligence, guilt proneness (are more apprehensive, self-reproaching, insecure), possibly also higher ergic tension and radicalism. The changes in other personality factors were manifested by difference in distribution of values of the factor rather than in differences in the mean values of the factor.

These changes, however, cannot be observed directly when the women are sorted into the Toxoplasma-negative and positive groups on the basis of routine serological tests (like CFT). These tests are optimised for early diagnosis of acute toxoplasmosis. They are able to prove the existence of high titres of specific anti-Toxoplasma antibodies which are characteristic for patients with an acute phase of acquired toxoplasmosis. In most of clinical laboratories the samples of sera are either measured from the titre 1 : 8 or the subjects with the titres less then 1 : 8 are considered as Toxoplasma-negative (and are excluded from further analysis by more specific tests, for example by IgM ELISA). The women in our experimental set were screened for toxoplasmosis during routine clinical examination in pregnancy. Their sera were tested by complement fixation test (Warren and Sabin 1942) and the subjects without positive reaction in 1 :8 dilution were considered as Toxoplasma-negative. The clinical records as well as the comparison of results of CFT and IgG ELISA tests suggests, that the titres of specific antibodies estimated by CFR can decrease below 1 : 8 within a few years after the end of acute toxoplasmosis. Therefore, our group of 136 Toxoplasma-negative women must be contaminated by an unknown percentage of women with old Toxoplasma gondii infection. The results of our observation of toxoplasmosis patients during the interval 13 years after infection (Flegr et al. 1996) showed that at least some of the Toxoplasma gondii induced personality changes are very slow. Therefore, the personality of subjects with longest infections (who might be often missdiagnosted as Toxoplasma-negative) can express the most prominent changes in our experimental set. Even a small percentage of such subjects in the Toxoplasma-negative set can flatten out the possible differences between the two subsets of women. In the first study (Flegr and Hrdý 1994) in which prominent differences between Toxoplasma-negative and Toxoplasma-positive were observed the toxoplasmin intradermal delayed hypersensitivity test (Feldman 1954) was used for diagnosis of latent toxoplasmosis. This old test monitors cellular rather then humoral immunity. The clinical experience shows that the positive reactions in the intradermal delayed hypersensitivity test persists for a very long time, probably for the whole life of an infected person (Remington and Krahenbuhl 1982). When the toxoplasmosis is diagnosed with a common serological test like CFT the presence of unknown percentage of false negatives must be anticipated and the existence of any differences between Toxoplasma-negative and Toxoplasma-positive subjects must be tested by proper statistical method (such as the permutation test with data reassignation).

In our study the permutation tests revealed the existence of differences in mean values of factors B, O, possibly also Q4 and Q1. In the factors F, L, N and Q3 the latent toxoplasmosis affected the distribution of personality factors= values, rather then their mean values. The lover kurtosis of the distribution as well as the absence of distinct peak in the histogram of the distribution can be explained by the fact that the Toxoplasma-induced personality shift is probably a long-lasting process. Our results (Flegr et al. 1996) suggest that the process is triggered by the infection, however, it takes many years to fully evolve. Consequently, the women with a relatively fresh infection are Toxoplasma-positive on the basis of serological tests, however, their personality profile has still the Toxoplasma-negative character. As our experimental set contains the women with toxoplasmosis of various length no distinct peak but rather a flat plateau can be observed on the histograms of personality factors of Toxoplasma-positive women. As we already discussed the absence of significant difference of mean values of the factor can be explained by missdiagnosis of the most changed subjects (with lowest antibody titres) as Toxoplasma-negative.

The results of present analysis of the set of young women slightly differ from those obtained on the set of students and teachers of biology of the Charles University (Flegr and Hrdý 1994, Flegr et al. 1996). They are, however, similar to those obtained on the set of acute toxoplasmosis patients and on the subset of 55 Toxoplasma-positive women (submitted). In the set of biologists the Toxoplasma-positive women had higher A (affectothymia), Q3 (strength of self sentiment), and lower L (protension). In the set of 230 women with clinical history of acute toxoplasmosis the duration of infection positively corelated with G (superego strength), and Q3 (strength of self sentiment) while in the set of 55 young women with latent toxoplasmosis the length of infection (estimated on the basis of antibody titres) positively corelated with A (affectothymia), F (surgence), G (superego strength), H (parmia) and L (protension). The differences between the results obtained on particular experimental sets can be probably explained by special nature of some of these sets. Especially the biologists represent a highly atypical population sample which differs in many personality traits from a general population. Despite the differences a similar set of personality factors (usually incorporating the factors A, F, G, L, O, Q3 and Q4) seems to by influenced by latent toxoplasmosis in all examined sets of women. The results of discrimination analysis and of logistic regression (Flegr and Hrdý 1994, Flegr et al. 1996) suggest that only some of these factors are influenced by the parasite directly while the others are changed because of their correlation with other (toxoplasmosis influenced) factors. As the correlation matrices of Cattells factors often differ among various social and professional groups, the changes in secondary-influenced factors might vary among different experimental sets.

The results of the current study are very important in two respects. First, in the comparison with all previous studies the experimental set represents a homogeneous sample of normal population of young women. The experimental set of biologists (Flegr and Hrdý 1994) represents highly untypical population of university students and teachers. The second experimental set (Flegr et al. 1996) is a relatively good representation of Czech population of women. However, the age-structure of the sample is highly heterogeneous. Moreover, all women in this sample experienced relatively severe acute toxoplasmosis disease (in contrast with most of other infected people they were diagnosed for acquired toxoplasmosis and received a medical help). In both cases it is not clear whether the results and conclusions can be extrapolated for normal population.

Secondly, in all previous studies the subjects were informed about the aim of the projects before the experiment. In this study neither toxoplasmosis nor T. gondii were mentioned in the cover letter (to avoid possible fear of young mothers of congenital toxoplasmosis). For the first time we fully excluded any possible intentional or unintentional distortion of data by the experimental subjects.

It is not possible to decide on the basis of present data whether the toxoplasmosis induces the changes in personality or whether the certain combination of the personality traits increases the probability of contact with T. gondii infection. There are, however, several reasons to believe that former possibility is the correct one: 1. Significant positive correlation exists between the duration of latent toxoplasmosis and the amount of personality shift in the sets of men (Flegr et al. 1996) and women (submitted) diagnosed with acute toxoplasmosis during the period of 13 and 14 years, respectively in various Prague hospitals. 2. Significant negative correlation exists between the level of anti-Toxoplasma antibodies (which indirectly reflects the duration of latent toxoplasmosis) and the amount of personality shift in the sets of biology students (Flegr and Hrdý 1994) and Toxoplasma-positive young women (submitted). 3. No correlation exists between the major toxoplasmosis-risk factors (consumption of raw meat and contact with cat) and the personality factors influenced by toxoplasmosis (Flegr et al. 1998). 4. All but one (factor O) personality factors influenced by toxoplasmosis are shifted in the opposite direction in Toxoplasma-positive men and women. It is difficult to explain how the oppositely changed factors can promote the same effect in men and women, namely the increase of probability of T. gondii infection.

It can be only speculated, whether the induction of personality changes in men is connected with an attempt of the parasite to manipulate the host behavior, or are only byproducts of a non-specific decline in the quality of host life (connected, for example, with Toxoplasma-induced general immunosupression).

Acknowledgements. This research was supported by the grant FRV© 1314/1997. We thank to Petr Kodym for his help with the data gathering and Monika Flegrová for an adaptation of the program TREEPT.
 
 

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