Alexithymia in oncologic disease: Association with cancer invasion and hemoglobin levels
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Annals of Clinical Psychiatry
Annals of Clinical Psychiatry 2011;23(2):125-130 Research Article
Alexithymia in oncologic disease: Association
with cancer invasion and hemoglobin levels
Antonino Messina, MD Background: The literature suggests that alexithymia is the result of
Anna Maria Fogliani, MD
individual differences and/or biological mechanisms. Both individual
Scuola di Specializzazione in Psichiatria differences and disease mechanisms may play a role among individuals
Università di Catania
with medical or surgical conditions. The relative weight of clinical and
Catania, Italy
individual differences factors related to alexithymia has not been stud-
Sergio Paradiso, MD, PhD
ied in patients with cancer. The purpose of this study was to examine
Department of Psychiatry
University of Iowa the extent to which individual differences in perceived stress and bio-
Iowa City, IA, USA logical markers of illness severity are associated with alexithymia among
patients with cancer.
Methods: Treated oncologic outpatients (N = 37) were assessed using the
20-item Toronto Alexithymia Scale and Perceived Stress Scale. Alexithymia
was examined in relation to perceived stress, tumor staging, and hemoglo-
bin levels.
Results: Among the patients studied, 34.2% endorsed the established cut-
off score (≥61) for alexithymia. Higher alexithymia scores were found in
patients with more advanced stages of cancer invasion. Alexithymia cor-
related directly with perceived stress and indirectly with hemoglobin lev-
els. Hemoglobin levels and cancer invasion significantly correlated with
alexithymia when controlling for perceived stress.
Correspondence
Conclusions: A significant component of alexithymia in cancer patients
Sergio Paradiso, MD, PhD may be construed as acquired. But awareness of health status influencing
University of Iowa perceived stress might partially mediate the role of cancer invasion and
Department of Psychiatry hemoglobin on alexithymia.
200 Hawkins Drive, W278 GH
Iowa City, IA 52242 USA
Keywords: alexithymia, cancer, hemoglobin, perceived stress, personal-
E-MAIL
ity, tumor staging
sergio-paradiso@uiowa.edu
AACP.com Annals of Clinical Psychiatry | Vol. 23 No. 2 | May 2011 125Alexithymia in oncologic disease
I n tro d u c t i o n Methods
Individuals with limited introspective capacity and a From March 2007 to June 2007, cognitively intact out-
cognitive style characterized by difficulty expressing patients (N = 37; 20 women) with solid and hemato-
emotions and distinguishing between emotions and logic malignancies were enrolled from the oncology
bodily sensations are commonly identified as alex- services of the Cannizzaro and Ferrarotto Hospitals in
ithymic.1 Alexithymia is associated with psychiatric Catania, Italy, based solely on their willingness to par-
disorders including substance,2 somatoform,3 panic,4 ticipate in the study and their ability to consent accord-
posttraumatic stress,5 and eating disorders6; and with ing to the Declaration of Helsinki. Malignancy type,
medical illnesses, such as gastrointestinal dysmotility,7 staging, and hemoglobin levels were extracted from the
hypertension,8 and inflammatory bowel syndrome.9 medical record at the time of alexithymia assessment.
Alexithymia is a stable personality trait (ie, primary Alexithymia was measured using the Italian version
alexithymia)10 but also can be acquired or secondary. of the Toronto Alexithymia Scale (TAS-20).24 The TAS-
Mechanisms for acquired alexithymia may be brain 20 is a well-validated, widely used scale that measures
damage,11 age-related gray matter reduction in the alexithymia.25 Cutoff scores are as follows: ≤50, no alexi-
anterior cingulate cortex (ACC),12 or dysfunction in the thymia; 51 to 60, borderline alexithymia; and ≥61, alexi-
interhemispheric transfer of information (eg, resection thymia.25 Severity of depression was measured using
of the corpus callosum).13,14 the Italian version of the Beck Depression Inventory-II
Malignancies have been associated with ele- (BDI-II), with scores as follows: 0 to 13, minimal depres-
vated levels of alexithymia.15 Whereas identifying risk sion; 14 to 19, mild depression; 20 to 28, moderate
factors for alexithymia in oncologic illness may help depression; and 29 to 63, severe depression.26,27
in targeting medical interventions and may ultimately Perceived stress was measured using the 10-item
lead to improved quality of life,16 research in this Perceived Stress Scale (PSS),28 a widely used instru-
area has been scant. The present study represents ment that measures stress perception for the previous
an initial step in identifying potential risk factors for month. Response options are assessed using a 5-level
alexithymia in cancer patients. It was posited that Likert scale (0, never to 4, very often). PSS scores range
alexithymia in oncologic disease may have primary from 0 to 40, with higher scores indicating greater stress.
(related to individual differences)10 and/or second- Moreover, each patient was assigned a cancer stage
ary (acquired or biological) mechanisms.11,17 As an according to the TNM classification, which consid-
individual difference factor, the choice fell on stress ers size and extent of tumor (T), involvement of lymph
because stress is perceived differently depending on nodes (N), and presence of metastasis (M).
the personality of the individual,18 and the degree to
which stress is perceived is considered a heritable Data analysis
psychological factor.19 In addition, the trying life con- The effects of sex and cancer type on alexithymia,
ditions of individuals with cancer invariably result perceived stress, and hemoglobin levels were exam-
in a wide range of stress responses, limiting foresee- ined for descriptive purposes using ranks (data were
able floor and ceiling effects on the perceived stress not normally distributed), and t and F statistics.
measure. Hypothesis testing (ie, associations of alexithymia with
As biological factors, anemia and degree of cancer hemoglobin level and perceived stress) was carried out
invasion were chosen because they are clear indicators using ranks, correlation, and regression techniques.
of illness severity.20 In addition, almost all individuals One-way analysis of variance (ANOVA) was used to
with cancer will develop some degree of anemia, with examine the effect of illness staging on ranked alexi-
up to 80% of patients experiencing serious hemoglobin thymia scores and hemoglobin levels. Least square
reduction.21-23 differences (LSD) were examined to report post hoc
This study examined the extent to which alexi- significant differences when the omnibus model
thymia among cancer patients is associated with psy- was significant. All analyses were carried out using
chological (ie, perceived stress) and/or biological (ie, the Statistical Package for the Social Sciences (SPSS)
anemia and tumor staging) factors. version 17.0.1.
126 May 2011 | Vol. 23 No. 2 | Annals of Clinical PsychiatryAnnals of Clinical Psychiatry
Table 1
Alexithymia, perceived stress, and hemoglobin levels by malignancy type
TASa PSSb Hemoglobinc
Cancer type n Mean SD Mean SD Mean SD
Hematologic 5 60.4 10.8 26.4 6.58 9.80 2.05
Gastroenteric 13 56.0 8.6 21.8 6.72 10.62 1.94
Genitourinary 6 55.5 5.8 19.2 2.99 11.17 1.83
Breast 10 48.5 10.2 19.6 5.87 11.20 1.55
Lungs 3 66.3 1.5 25.3 2.52 9.67 2.08
TOTAL 37 55.35 9.78 21.46 6.00 10.68 1.83
aANOVA for TAS: F(4,32) = 3.6; P < .02.
bANOVA for PSS: F(4,32) = 2.6; P = .051.
cANOVA for hemoglobin level: F(4,32) = .8; P > .4.
Post hoc analyses: Patients with hematologic malignancies (LSD = 12.2; P < .03) and lung malignancies (LSD = 22; P = .001) showed significantly higher alexithymia compared
with patients with breast cancer.
ANOVA: analysis of variance; LSD: least squares difference; PSS: Perceived Stress Scale; SD: standard deviation; TAS: Toronto Alexithymia Scale.
R e s u lt s were not different from mean values for women (10.3
mg/dL; SD = 1.6) (t = 1.4; df = 36; P > .2).
The patients’ age range was 32 to 75 years (mean age, Effects of malignancy type on alexithymia, perceived
59.8; SD = 10.2). Most patients (84.2%) were married, stress, and hemoglobin levels were examined for descrip-
15.8% were single or widowed; the mean education was tive purposes (Table 1). A significant effect of cancer type
10.9 years (SD = 4.8); and employment was as follows: on alexithymia was found (F[4,32] = 3.6; P < .02), while
5.3%, primary sector; 13.2%, secondary sector; 39.5%, the effect on perceived stress just failed to meet signifi-
tertiary sector; and 26.3%, retired. According to the cance (F[4,32] = 2.6; P = .051) and there was no significant
BDI-II cutoff scores, 4 participants (10.8%) had moder- effect of cancer type on hemoglobin level (F[4,32) = .8;
ate depression, and 14 (37.8%) had severe depression. P > .4). Patients with breast cancer had the lowest alexi-
Patient malignancies were as follows: 13, gastroenteric; thymia scores, whereas patients with lung cancer had the
10, breast; 6, urogenital; 5, hematologic; and 3, pulmo- highest alexithymia scores (Table 1). Patients with hema-
nary. Proportions of patients by TNM staging were as tologic (LSD = 12.2; P < .03) and lung malignancies (LSD
follows: stage I, 5.4%; stage II, 43.2%; stage III, 37.8%; = 22; P = .001) showed significantly higher alexithymia
and stage IV, 13.5%. Patients with hematologic cancer compared with patients with breast cancer. No other dif-
were at stage II (80%) or III (20%); patients with gastro- ferences were found to be statistically significant.
enteric cancer were at stage II (31%), stage III (46%), or The influence of stage of tissue invasion on alexi-
stage IV (23%); patients with breast cancer were at stage thymia, perceived stress, and hemoglobin levels are shown
I (20%), stage II (40%), stage III (20%), or stage IV (20%); in Table 2. The effect of cancer invasion on alexithymia was
patients with urogenital cancer were at stage II (80%) or statistically significant (F[3,33] = 5.8; P = .002) and showed
stage III (20%); and all pulmonary cancer patients were that alexithymia scores were higher with greater tissue
at stage III. invasion (see Table 2 for details on post hoc analyses). The
Prevalence of alexithymia (TAS-20 ≥61) was 34.2%. effect of cancer staging on perceived stress also was signifi-
Mean alexithymia score was 55.3 (SD = 9.7; range, 40 to cant (F[3,33] = 3.5; P = .025) (see Table 2 for details on post
79). For women, the mean score was 54.4 (SD = 11.5) hoc analyses). The effect of cancer staging on hemoglobin
and for men it was 56.5 (SD = 7.4) (t = .63; df = 36; P > level just failed to reach statistical significance (F[3,33] =
.5). Mean perceived stress was 21.6 (SD = 6.0), with men 2.7; P = .063). When patients with hematologic cancer (n
showing a mean of 21.5 (SD = 5.5) and women show- = 5) were excluded from the analysis, the effect of cancer
ing 21.7 (SD = 6.5) (t = –.11; df = 36; P > .4). Hemoglobin staging on hemoglobin level became statistically signifi-
mean values were 10.7 mg/dL (SD = 1.8; range, 8 to 14 cant (F[3,28] = 3.5; P = .028), confirming that stage of cancer
mg/dL). Mean values for men (11.1 mg/dL; SD = 1.9) invasion and anemia are related indices of illness severity.
AACP.com Annals of Clinical Psychiatry | Vol. 23 No. 2 | May 2011 127Alexithymia in oncologic disease
Table 2
Alexithymia, perceived stress, and hemoglobin levels by cancer staging
TASa PSSb Hemoglobinc
Cancer stage n Mean SD Mean SD Mean SD
I 2 44.0 0 10.50 0.71 10.50 .71
II 16 50.9 2.3 21.31 5.03 11.56 1.82
III 14 59.0 1.9 20.17 5.89 9.86 1.56
IV 5 63.6 4.2 26.20 5.72 10.20 1.92
TOTAL 37 55.35 9.78 21.66 6.05 10.68 1.83
aANOVA for TAS: F(3,33) = 5.8; P = .002.
bANOVA for PSS: F(3,33) = 3.5; P = .025.
cANOVA for hemoglobin level: F(3,33) = 2.7; P = .063.
Post hoc analyses for TAS showed significant differences between stages I and III (LSD = 18; P < .02) and I and IV (LSD = 21.6; P .5).
Post hoc analyses for PSS showed significant differences between stages I and III (LSD = 17.6; P < .03) and I and IV (LSD = 25.7; P < .005) and between stages II and IV (LSD =
10.9; P < .04). No significant difference was found between stages I and II (LSD = 14.8; P = .055) or between III and IV (LSD = 8.0; P =.13).
ANOVA: analysis of variance; LSD: least squares difference; PSS: Perceived Stress Scale; SD: standard deviation; TAS: Toronto Alexithymia Scale.
Hemoglobin level inversely correlated with alexi- sion, and hemoglobin level together accounted for about
thymia (r = –.51; P = .001) and with perceived stress (r = 50% of the variance in alexithymia. Hemoglobin level and
–.42; P = .005), which directly correlated with alexithymia cancer staging were significant predictors of alexithymia,
(r = .52; P = .001). When patients with hematologic cancer independent of perceived stress.
were excluded, correlations between hemoglobin levels
and alexithymia remained essentially the same (r = –.49;
P = .004; n = 32) as well as the association between alexi- Discussion
thymia and perceived stress (r = .50; P = .003; n = 32), but
the correlation between hemoglobin level and perceived The present study found a 34.2% prevalence of alexi-
stress was no longer significant (r = –.27; P > .1; n = 32). thymia in cancer patients. This is consistent with the 36.4%
These 2 sets of analyses indicate that lower hemoglobin prevalence found in women with breast cancer15 and is
levels predicted severity of alexithymia, which was also about 8-fold greater than in the general population of Italy
associated with perception of stress, but in nonhema- (4.5%).9 There is broad consensus that alexithymia may
tologic oncologic disease, perceived stress was not pre- stem from individual developmental differences,10 age-
dicted by anemia. related brain changes,12 or medical or surgical disease.17
Perceived stress, cancer staging, and hemoglobin In this sample of cancer patients, psychological factors (ie,
level were then examined in a regression model predict- stress perception) accounted for about 30% of the variance
ing alexithymia. The model showed an overall r = .70 (R2 in alexithymia. Hemoglobin level and degree of cancer
= .49) (F[3,33] = 10.6; P < .0001). Standardized beta for invasion were independently associated with alexithymia,
perceived stress was .25 (t[1,36] = 1.7; P > .10), while for and each accounted for an additional 10% of the variance.
cancer staging it was .37 (t[1,36] = 2.6; P < .02), and for In addition, cancer invasion and lower levels of hemoglo-
hemoglobin it was –.29 (t[1,36] = –2.05; P < .05). Perceived bin were associated with greater perceived stress. When
stress, hemoglobin, and cancer staging were also entered patients with hematologic cancer were excluded from the
independently in the hierarchical model. In this case, the analysis, the association of low hemoglobin levels with
R2 for perceived stress was .29 (F[1,35] = 14.4; P = .001), perceived stress was no longer significant. These findings
whereas the R2 changed to .38 after hemoglobin (F[1,34] confirm that overall health status has significant implica-
= 5.1; P < .05) was entered, and to .49 (F[1,33] = 6.9; P < tions on psychological well-being. We do not know how
.02) after cancer staging was entered. The order in which many patients were fully aware of their survival prognosis
the independent variables were entered did not affect based on their cancer progression, which raises the possi-
the results. In summary, perceived stress, cancer inva- bility that illness severity and perceived stress were at least
128 May 2011 | Vol. 23 No. 2 | Annals of Clinical PsychiatryAnnals of Clinical Psychiatry
in part associated because of the patients’ knowledge of phocytes induce the proliferation of lymphocytes, CD8+,
their prognosis. and natural killer cells and therefore may have an impor-
Some limitations should be acknowledged before tant role in stimulating cell-mediated defense against
further discussion of the findings in this study. The sam- cancerous cells. On the other hand, alexithymia may be a
ple size was limited, and enrollment was notably influ- psychological consequence of stress and suffering,36 com-
enced by patients’ willingness to take part in the study. mon especially in advanced stages of tissue invasion. The
These findings—including the association between can- present study has shown that in addition to these psycho-
cer type and alexithymia—will need replication with a logical mechanisms, cancer may play a significant role in
larger, randomly selected sample of patients. In addition, alexithymia by altering the normal somatic physiology,
the sample size limited the number of possible analyses. through both invasion of healthy tissue and anemia.
Only the TAS-20 total score, and not the 3 factors—dif- The ACC, a cerebral structure involved in the mech-
ficulty identifying emotions, difficulty describing emo- anisms of alexithymia,12,37-39 is among the brain regions
tions, and externally oriented thinking—was examined, most vulnerable to hypoxic injury.40 In humans, the ACC
and no analyses were conducted to explore the associa- shows early functional decline,41 perhaps due to vascular
tion of alexithymia and its factors with depressive symp- vulnerability.42 Decline in function and structure of the
toms. This association has been examined extensively in ACC has been considered a mechanism for the greater
the literature, showing that overlap and independence of degree of alexithymia observed in older age.12 Therefore,
the 2 constructs exist.29,30 a potential mechanism by which hemoglobin is associ-
Similarly, the number of psychological illness sever- ated with alexithymia is a reduction of oxygen transport
ity factors was limited. A different set of illness severity to the brain and, specifically, to the anterior cingulate.12,42
predictors may have yielded different results. No longitu- The corpus callosum also has been posited as a brain
dinal measures of alexithymia were available, allowing a structure involved in alexithymia.43,44 This important
definite causal association with biological or psychologi- route of interhemispheric communication also is vulner-
cal factors. In this regard, contrary to the implications of able to low oxygen, as hypobaric hypoxia affects the mor-
the results of the present study, relative stability of alexi- phologic and functional maturation of the corpus callo-
thymia in cancer has been reported.31 In that study, sta- sum in rats during postnatal development.45
bility of alexithymia was suggested based on an initial The findings of the present study confirm the well-
evaluation carried out the day before surgery and another established and general notion that lower hemoglobin
evaluation attained 6 months after surgery; no measures levels are associated with impaired psychological func-
of illness severity were reported at the initial or follow-up tioning.46 It is noteworthy that correction of low hemo-
evaluations.31 A longitudinal design with assessment of globin levels with iron therapy improves cognitive per-
alexithymia before onset of the malignancy may resolve formance in otherwise healthy adults.47 The hypothesis
this question. that treatment of anemia improves alexithymia warrants
In addition, the findings in the present study may not empirical testing. Improvement of alexithymia with
generalize to childhood malignancies, as 5-year cancer relatively simple interventions aimed at reducing ane-
survivors (diagnosed before age 19) showed no signifi- mia may alleviate the negative effects of alexithymia on
cant differences in alexithymia compared with healthy immune response.
comparisons, and no indication of medical severity—not In summary, patients with cancer in the present
including hemoglobin levels—was found to be associ- study showed greatly elevated rates of alexithymia in rela-
ated with alexithymia.32 tion with rates in the general population.9 Alexithymia
The relationship between alexithymia and cancer is was associated with progression of cancer invasion.
complex and bidirectional. By altering the expression of Alexithymia correlated directly with perceived stress and
immune function, alexithymia may have a role in the eti- indirectly with hemoglobin levels. Hemoglobin levels
ology of cancer.33 Levels of IL-1β, IL-2, and IL-4 and TH1/ and cancer invasion significantly correlated with alexi-
TH2 lymphocytes (IL-2/IL-10) and CD4:CD8 ratios, as thymia when controlling for perceived stress. Perceived
well as CD4, are decreased in women with alexithymia.34 stress, strongly influenced by personality, was associated
This may in part be the indirect result of elevated steroid with cancer invasion but less definitively with lower levels
response to stress as a function of alexithymia.35 TH1 lym- of hemoglobin. These findings suggest that alexithymia
AACP.com Annals of Clinical Psychiatry | Vol. 23 No. 2 | May 2011 129Alexithymia in oncologic disease in cancer patients can be viewed as partly acquired and by the Edward J. Mallinckrodt, Jr. Foundation Grant potentially amenable to improvement with treatment of Program, the Dana Foundation, and a National Institutes the underlying medical condition. ■ of Health Career Development Award (5K23AG027837). Acknowledgments: The authors thank Dr. Natalie Disclosures: The authors report no financial relation- Denburg and Dr. Susan Schultz for their helpful com- ship with any company whose products are mentioned in ments on the manuscript. Dr. Paradiso was supported this article or with manufacturers of competing products. References 1. Apfel RJ, Sifneos PE. Alexithymia: concept and mea- Psychosom Med. 2001;63:944-950. 33. Dewaraja R, Tanigawa T, Araki S, et al. Decreased surement. Psychother Psychosom. 1979;32:180-190. 18. 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