Psychiatry Research 256 (2017) 412–416

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Psychiatry Research
journal homepage: www.elsevier.com/locate/psychres

Iris structure and minor physical anomalies in schizophrenia MARK

⁎
Dániel Trixler , Tamás Tényi
Department of Psychiatry and Psychotherapy, University of Pécs, Faculty of Medicine, Rét u.2.H, 7623 Pécs, Hungary

A R T I C L E I N F O A B S T R A C T

Keywords: This study compared five human iris characteristics and minor physical anomalies (MPAs) between patients with
Schizophrenia schizophrenia (n = 32) and controls (n = 31). Correlations between iris characteristics and MPAs were ex-
Iris pected, due to their same ectodermic origin. Iris macro photos were taken and quantified in five categories
Iris structure mentioned before. MPAs were also examined in both groups. Our results show significant differences in the
Minor physical anomalies
frequency of pigment dots of the iris and total number of MPAs between groups. Other significant differences
Phenotype
Biological markers
were found in the extension of concentric furrows, as they were more common in healthy subjects, while
Wolfflin nodules occurred significantly more often in patients with schizophrenia. Expected difference in Fuch's
crypts could not be observed between groups. Light eye color was positively correlated to pigment dots and
Wolfflin nodules, and negatively correlated with concentric furrows. Dark eye color showed positive correlation
with concentric furrows, and negative correlation with pigment dots and concentric furrows. A gender effect
could also been observed: male individuals showed moderate positive correlations between pigment dots and
total MPAs frequency, while this couldn’t be observed in the female group. Our findings suggest possible con-
nections between iris characteristics and MPAs, where males are more prone to deviations.

1. Introduction
1.1. Minor physical anomalies and schizophrenia
Minor physical anomalies (MPAs) are mild cosmetical errors of the
skin which are results of insignificant errors of morphogenesis in pre-
natal stage (Pinsky, 1985). These MPAs could serve clinicians as a va-
luable indicator of altered morphogenesis in early gestation. Review of
the literature gathered a significant amount of evidence demonstrating
that people with neurodevelopmental disorders show elevated pre-
valence of MPAs compared to controls (Tényi et al., 2009). According to
two meta-analysis numerous studies report an increased frequency of
MPAs in schizophrenic groups compared to controls (Weinberg et al.,
2007; Xu et al., 2011). There is also a possible hereditary factor. A
recent study found that MPAs were more common in the head and
mouth regions among the relatives of schizophrenia patients compared
to normal controls (Hajnal et al., 2016).
that the ACC's functions can be separated into two main parts. The
anterior part is associated with emotion regulation and motoric func-
tions, while the posterior part plays a role in visuospatial and memory
processing (Bush et al., 2000). The cingulate cortex functions both as
filter and amplifier, where the cognitive and affective components are
linked together (Devinsky et al., 1995). The cingulate cortex plays an
additional role in the regulation of attention and error control. It is
possible that this area plays a role in disorders such as OCD, anxiety or
excessive impulsivity if the ratio of emotional signal amplification is not
appropriate (Bushet al., 2000). The ACC is also involved in pain per-
ception. Lesions to this area reduce pain sensation. The patient is
conscious of the painful stimuli, but it does not provoke a negative
emotional reaction, and therefore it does not disturb him. (Folz and
White, 1962). In regards to schizophrenia a meta-analysis of 7 studies
showed reduced volume of the ACC in schizophrenia group compared
to controls (Baiano et al., 2007), showing a neurodevelopemental
background.

1.2. Anterior cingulate cortex and schizophrenia 1.3. Human iris, PAX6 and the ACC

In recent decades we can see an increasing emphasis in cognitive Studies confirm that Pax6 is a likely candidate gene for tissue dif-
neuroscience on a particular part of the limbic system, the anterior ferences in the iris. Pax6 dosage influence the muscle-cell differentia-
cingulate cortex (ACC). Earlier conceptions attributed a single function tion in the iris (Jensen, 2005). Davis-Silberman et al. (2005) conclude
to this region: regulation of emotions. Subsequent studies have shown that iris stroma defects are likely to be due to cell non-autonomous

⁎
Corresponding author.
E-mail address: daniel.trixler@aok.pte.hu (D. Trixler).

http://dx.doi.org/10.1016/j.psychres.2017.07.004
Received 17 March 2017; Received in revised form 15 May 2017; Accepted 3 July 2017
Available online 05 July 2017
0165-1781/ © 2017 Elsevier B.V. All rights reserved.
D. Trixler, T. Tényi
events, where Pax6 regulates the expression of the cells which are re-
quired for the adhesion of the iris stroma. Thus, it is possible that Pax6,
Six3 and Lmx1b which influence the growth of the precursors to the cell
layers in the iris, could influence the variability of crypts and con-
traction furrows typically present in peoples irises. The link between
Pax6 and the anterior cingulate cortex has been already researched.
One study demonstrated that family members with a mutation in
Pax6showed high rates of unusual behavior, including disinhibition,
impulsive behavior, impaired social understanding and impaired verbal
inhibition (Heyman et al., 1999). A later study used magnetic resonance
imaging (MRI) in this family (Ellison-Wright et al., 2004) and found
local gray and white matter changes in the anterior cingulate cortex
(approximate Brodmann area 24, 32), as well as posterior white matter
abnormalities in the corpus callosum extending posteriorly into the
cingulate cortex, which are brain areas that have been associated with
personality traits (Davidson, 2001; Johnson et al., 1999; Posner and
Rothbart, 1998).
1.4. Iris and personality
Larsson et al. (2007) pioneering study found significant correlations
between iris structures and personality using the revised NEO person-
ality inventory (NEO-PI-R), especially regarding to Fuchs crypts and
concentric furrows. Larsson reported that people with many concentric
furrows (also called nerve rings) were found to have a low ability to
control impulses compared to people with few nerve rings. Results of
Lim et al. (2014) show that psychological trait perseverance has a ne-
gative correlation with the grade of concentric furrows, which is con-
sistent with Larsson's previous result. However, development of the
concentric furrows not only has a negative correlation with persever-
ance, but also has a positive correlation with novelty seeking. In-
dividuals high in novelty seeking tend to be excitable, exploratory, and
easily bored, and those low in perseverance tend to give up easily when
faced with frustration, criticism, obstacles, and fatigue. Although the
above mentioned data are known on the connection between the iris
structure and personality characteristics, no study was reported on the
relationship between the iris characteristics and specific psychiatric
disorders (schizophrenia, mood disorders, personality disorders).
1.5. The role of timing in the formation of iris structures
Fuch's crypts are patch like atrophies in the two top cell layers in the
iris, the anterior border layer and underlying stroma. They are formed
sometime between the third and eight month of gestation and are
present at birth (Oyster, 1999). On the other hand, pigment dots can be
rarely seen on the surface of the anterior border layer of the iris before
the age of six (Eagle, 1988). Iris characteristics originating from the
same cell layers generally share genetic factors. Examples are contrac-
tion furrows, which become manifest due to the iris folding in the same
location when the iris aperture adapts to different light conditions. The
overall thickness and density of the iris influence the extension and
distinction of contraction furrows. Looking at iris color, the more pig-
mented iris also contributed to increased extension and distinction of
contraction furrows, which indicated that the amount of melanin that is
present in the iris increases its overall density (Larsson and Pedersen,
2004). A comprehensive recent study (Edwards et al., 2016) describes
the distribution of the main iris features such as pigment spots, Fuchs’
crypts, Wolfflin nodules or contraction furrows in large populations of
European, East Asian and South Asian ancestry. After analyzing 1465
irises belonging to different people, the survey conclude that the dis-
tribution of iris features is very population dependent. They found that
all traits showed significant differences in frequency across the three
groups.
1.5.1. Four hypotheses were tested
First hypothesis was that both iris structures and MPAs are markers
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Psychiatry Research 256 (2017) 412–416
of neurodevelopment and there are significant differences between the
schizophrenic and control group according to the frequency of Fuchs
crypts, concentric furrows, Wolfflin nodules, pigment dots and minor
physical anomalies. Theory behind the hypothesis is that a denser iris is
expected more in healthy individuals, meaning low number of Fuchs
crypts. While Fuchs crypts are regions with missing iris tissue, on the
other hand contraction furrows are often results of the iris folding at the
same spots when the pupil is expanding. Generally thicker irises are
more prone to have visible folding marks. A higher number of Wolfflin
collagen nodules and minor anomalies are expected in the schizo-
phrenic group, mainly because of the same ectodermic origin of the iris,
skin and central nervous system.
Second hypothesis assumed that there could be correlations be-
tween the frequencies of Fuchs crypts, concentric furrows, Wolfflin
nodules, pigment dots and minor anomalies at the individual level. If
there are significantly more crypts, nodules, pigment dots and minor
anomalies in the schizophrenic group, there is a possibility that on an
individual level we see aggregation of abnormalities.
Third hypothesis supposed that there will be a significant gender
difference, where males are more likely to show deviation from average
structural patterns, as other studies showed that iris characteristics are
affected by gender (Lim et al., 2014).
Fourth hypothesis assumes positive correlations between lighter iris
color and Wolfflin nodules and negative correlation with concentric
furrows. Prior research suggests that Wolfflin nodules are more
common in people with light eye color. It is also anticipated that darker
irises are on average thicker than light colored ones and a thicker iris is
more prone to folding, which causes concentric furrows.
2. Subjects and methods
The purpose of the study was to examine whether there is a quan-
tifiable difference between the iris characteristics and minor physical
anomalies of healthy and schizophrenia individuals in a Caucasian
(Hungarian) sample. Macro iris photos of 31 healthy and 32 schizo-
phrenic patients were used in the statistical analysis. The diagnosis of
the schizophrenia patients were evaluated by the use of the DSM-5
(American Psychiatric Association, 2013). Patients with other neu-
ropsychiatric disorders were excluded from the study, controls were
healthy volunteers. No data on the family history of patients and
healthy controls relating to psychoses were available. As we were in-
terested in the correlations of the two trait markers (iris structure and
MPAs), the evaluation of other clinical characteristics (positive and
negative symptoms, age of onset) were not included in this study.
Photos were taken from 30 cm distance with a 90 mm fix-focused
macro lens. The structures were categorized with reference photos
taken from Larsson's former study of iris structures and personality
(Larsson and Pedersen, 2004). The examination of iris structures and
MPA's were evaluated by two independent researchers. Before the sta-
tistical analyses inter-rater reliability was tested and the kappa coeffi-
cient was > .75 for all items. Iris structures examined in this study were
Fuchs crypts, concentric furrows, Wolfflin nodules and pigment dots.
Regarding the examination of MPAs we have used the Méhes Scale
for evaluation, which includes 57 minor signs (Méhes, 1988). Minor
physical anomalies are connected to body regions for comparison and
analysis of data. A clear differentiation between minor malformations
and phenogenetic variants were introduced, the scale and detailed de-
finitions were published earlier (Trixler et al., 1997, 2001; Tényi et al.,
2004). All participants gave informed consent; the study was performed
in accordance with the Declaration of Helsinki and was evaluated fol-
lowing institutional guidelines. The examination of minor physical
anomalies was done qualitatively (present or absent) without scores
being used, but where it was possible, measurements were taken with
calipers and tape to improve the objectivity of examination. (Tényi
et al., 2015).
D. Trixler, T. Tényi Psychiatry Research 256 (2017) 412–416

Fig. 1. Examples of the studied iris structures. Different individuals’ irises have been paired to demonstrate the two endpoints of the categorizing scale, from left to right: Fuch's crypts,
pigment dots, concentric furrows, Wolfflin nodules.

3. Statistics Table 1
Differences in iris characteristics and MPAs between schizophrenia and control group.
To examine mean differences between the two groups we used
Schizophrenia Control Test of Asymp.
Mann-Whitney U test for ordinal scales (frequency of Fuchs Crypts, (n = 32) (n = 31) difference Significance
concentric furrows, Wolfflin nodules and pigment dots), for nominal (2-tailed)
scales Chi-square test were used (gender, eye color). To determine Mean Rank Mean U p
possible correlations between iris structures and MPA's, Pearson's cor- Rank
relation test was initialized. The level of significance was determined as Fuch's crypts 32.27 31.73 487.500 .903
p = 0,05 (2-tailed). Statistics were executed with IBM SPSS Statistics Concentric 27.63 36.52 356.000 .047*
22.(Fig. 1) furrows
Pigment dots 36.64 27.21 347.500 .041*
Wolfflin 36.16 27.71 363.000 .039*
nodules
4. Results Total MPAs 44.09 19.52 109.000 .000**

No significant differences were found in the mean age of the schi- *Difference is significant at level p ≤ .05.
zophrenia group (41) and the controls (37). Also no significant differ- **Difference is significant at level p ≤ .001.
ences were observed when using Chi-Square test between the schizo-
phrenic and control group regarding gender. χ2(1) = 131.2, p = .244.
Table 2
Male to female ratio in schizophrenic group was 20-12, control group Differences in iris characteristics and MPAs between schizophrenia and control group
15–16. using gender as a subdivision.

Male Sch. Male Con. Test of Exact significance

(n = 20) (n = 15) difference [2*(1-tailed)]
4.1. Iris and MPAs Mean Rank Mean Rank U p

Using Mann-Whitney test the frequency of Fuch's crypts between the Fuch's crypts 16.53 19.97 120.500 .330
two groups were not significantly different but regarding to the con- Concentric 14.80 22.27 86.000 .033*
furrows
centric furrows we saw a significant difference. We also observed sig-
Pigment dots 22.88 11.50 52.500 .001**
nificant difference in frequency of Wolfflin nodules. Pigment dots and Wolfflin 20.45 14.73 101.000 .107
MPAs, they were more common in patients with schizophrenia (see nodules
Table 1). Total MPAs 23.55 10.60 39.000 .000**

Female Sch. Female Test of Exact significance

(n = 12) Con. (n = difference [2*(1-tailed)]
4.2. Effects of gender 16)
Mean Rank Mean Rank U p
Fuch's crypts 16.17 13.25 76.000 .328
By splitting cases using gender only male patients showed sig- Concentric 13.50 15.25 84.000 .566
nificant differences using exact significance due to smaller sample size. furrows
Male subjects with schizophrenia showed significantly more pigment Pigment dots 14.21 14.72 92.500 .871
dots than the male controls. Concentric furrows were also significantly Wolfflin 16.04 13.34 77.500 .334
nodules
more common in the male control group.
Total MPAs 20.92 20.92 19.000 .000**
By looking at the data of total MPAs, males with schizophrenia had
higher numbers of total MPAs than the control male subjects. Females *Difference is significant at level p ≤ .05.
on the other hand showed only significant difference in the aspect of **Difference is significant at level p ≤ .001.
total MPAs between schizophrenic and control group (see Table 2).

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D. Trixler, T. Tényi Psychiatry Research 256 (2017) 412–416

Table 3 that iris of males are more affected. Another difference was shown in
Differences in iris characteristics and MPAs between dark and light eye colored subjects concentric furrows. Healthy subjects had them more often and it ne-
regardless of mental status and original grouping criteria.
gatively correlated with frequency of Wolfflin nodules. A near sig-
Dark Light Test of Asymp. Significance nificant negative correlation with number of pigment dots shows that a
(n = 27) (n = 36) difference (2-tailed) high number of concentric furrows could be indicator of a thicker iris
Mean Mean U p with less pigment dots and Wolfflin nodules. Regarding eye color, we
Rank Rank found similar results as prior studies in the aspect that Wolfflin nodules
Fuch's crypts 31.28 32.54 466.500 .777 are more common in people with lighter eye color (Larsson et al., 2007;
Concentric 44.39 22.71 151.500 .000** Davidson et al., 2010). We also found that pigment dots were more
furrows common in people with light irises and concentric furrows were more
Pigment dots 25.13 37.15 300.500 .010* common in participants with darker irises. Despite the schizophrenia
Wolfflin nodules 26.31 36.26 332.500 .016*
group had fewer individuals with light eye color, we observed more
Total MPAs 34.41 30.19 421.000 .356
pigment dots and Wolfflin nodules between them, which further re-
*Difference is significant at level p ≤ .05. inforce the results of this study. It is important to point out that schi-
**Difference is significant at level p ≤ .001. zophrenia is a complex spectrum of conditions and is associated with
many differences throughout the brain. It can be difficult to make
specific links between brain areas and the symptoms that are often
4.3. Effects of eye color observed. A meta-analysis done by Glahn et al. (2008) found that pa-
tients had reduced gray matter density relative to control subjects in
Using eye color categories dark and light, the distribution in Mann- many regions, including bilateral insular cortex, anterior cingulate, left
Whitney test revealed significant differences in pigment dots, con- parahippocampal gyrus, left middle frontal gyrus, postcentral gyrus,
centric furrows and Wolfflin nodules. Darker eyed subjects had lower and thalamus. Also some patients had increased gray matter density in
number of pigment dots. Results revealed also a lower rate of Wolfflin striatal region. From these findings we can see that schizophrenia in-
nodules in subjects with dark eye color. This is in correlation with prior volves many brain regions not only the ACC, but the losses in the
studies which indicated that Wolfflin nodules are more common in density of the iris have been only associated with the ACC so far,
lighter colored irises (Williams et al., 2011). It is noteworthy that while through the Pax6 gene expression.
there was no difference using Chi-Square test in eye color between the A caveat of the study, that due to the relatively small sample, the
two groups, there were more light eyed participants in the control effect of diagnosis, gender and eye color upon the studied variables
group. Schizophrenia group had 15 dark and 17 light eyed subjects, (MPAs and iris characteristics) was analyzed separately, multifactorial
while the control group ratio was 12 dark and 19 light eyed. Other analysis could not be done because of the sample size.
finding was a higher rate of concentric furrows in dark eyed subjects, Conclusion: To our knowledge this is the first ever study which
which supports the idea that darker irises with more layers of mela- examines the iris structural patterns of schizophrenia patients in rela-
nocytes are thicker and thus more prone to folding, which causes tion to minor physical anomalies, compared to healthy controls. Results
concentric furrows (Davidson et al., 2010) (see Table 3.) revealed significant differences in frequency of iris patterns and MPAs
between the two groups. A gender effect could also be observed, both in
4.4. Correlations iris structures and MPAs. This is in correlation with prior studies where
males showed more MPAs (Sivkov and Akabaliev, 2003) and iris
By searching for correlations in the whole sample, we utilized structural deviations (Lim et al., 2014). When looking for a higher
Spearman's rank order correlation which demonstrated a weak negative frequency in Fuch's crypts, focus should be directed to mental health
correlation between concentric furrows and Wolfflin nodules (rs (63) = problems that are also linked to decreased tissue volume in the ACC,
−.347, p = .005) and a near significant negative correlation between like impulse control disorders, where the diagnostic category doesn’t
concentric furrows and pigment dots (rs (63) = −.238, p = .060). show such a wide spectrum as in the case with schizophrenia. Our
Expected correlations between iris categories and MPAs were only re- findings suggest concentric furrows, Wolfflin nodules and pigment dots
vealed by splitting all cases using gender. Males showed moderate po- could also serve as possible biomarkers. Because of the topics novelty
sitive correlations between frequency of pigment dots and total minor the results indicate that there is potential and need for further research
anomalies (rs (63) = −.552, p = .001), while a significant difference in this area, especially with a higher number of subjects.
could not been observed in the female group.
Conflict of interest
5. Discussion
We report no conflict of interest.
Regarding the first hypothesis, results revealed significant differ-
ences in the frequency of concentric furrows, Wolfflin nodules, pigment Acknowledgments
dots and total MPAs between the two groups. The expected difference
was not significant when examining the frequency of Fuchs crypts. This study was supported by the National Brain Research Program
From Larsson's prior study we expected that we see most changes in (Grant no. KTIA-13-NAPII/12).
Fuchs crypts which have the strongest genetic predisposition (Larsson
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