Psychology, Health & Medicine

ISSN: 1354-8506 (Print) 1465-3966 (Online) Journal homepage: http://www.tandfonline.com/loi/cphm20

Is there an association between severity of illness

and psychiatric symptoms in patients with chronic
renal failure?

D. Guenzani, M. Buoli, G. S. Carnevali, M. Serati, P. Messa & S. Vettoretti

To cite this article: D. Guenzani, M. Buoli, G. S. Carnevali, M. Serati, P. Messa & S. Vettoretti
(2018): Is there an association between severity of illness and psychiatric symptoms in patients with
chronic renal failure?, Psychology, Health & Medicine, DOI: 10.1080/13548506.2018.1426868

To link to this article: https://doi.org/10.1080/13548506.2018.1426868

Published online: 15 Jan 2018.

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Psychology, Health & Medicine, 2018
https://doi.org/10.1080/13548506.2018.1426868

Is there an association between severity of illness and

psychiatric symptoms in patients with chronic renal failure?
D. Guenzania, M. Buolia  , G. S. Carnevalia, M. Seratia, P. Messab and S. Vettorettib
a
Department of Psychiatry, University of Milan, Fondazione IRCCS Ca’Granda Ospedale Maggiore Policlinico,
Milan, Italy; bUnit of Nephrology Dialysis and Renal Transplantation, Fondazione Ca’ Granda Ospedale
Maggiore Policlinico di Milano, Milano, Italy

ABSTRACT ARTICLE HISTORY

Chronic renal failure (CRF) is a frequent condition in elderly Received 3 March 2017
subjects, and it is associated with psychiatric comorbidity, especially Accepted 8 January 2018
depressive symptoms. Purpose of the present research was to KEYWORDS
compare patients with different severity of chronic kidney disease Consultation/Liaison
(CKD) in terms of psychiatric symptoms. One hundred CKD subjects psychiatry; depression;
were randomly selected among those attending the Department cognitive impairment;
of Nephrology, University of Milan. The patients were evaluated quality of life (QOL); physical
through the following rating scales: Mini-Mental State Examination illness
(MMSE), Beck Depression Inventory (BDI), Symptom Checklist
(SCL-90), Kidney Disease Quality of Life- Short Form (KDQOL-SF)
and Cumulative Illness Rating Scale (CIRS). A multivariable linear
regression analysis was performed considering eGFR as continuous-
dependent variable and rating scale scores as independent variables.
A worse eGFR significantly correlated with the score about the effects
of kidney disease on daily life (r = 0.25, p = 0.01) and the burden of
kidney disease (r = 0.18, p = 0.05). Statistical significance of kidney
disease on daily life persisted also in the final multivariate model
(t = 2.04, p = 0.04). Severity of renal dysfunction seems to influence
few psychiatric outcomes, particularly those related to quality of
life and daily functioning. This result might depend on the over-
worrying derived from the necessity to start a renal replacement
therapy in the near future.

Background
Psychiatric disorders are highly prevalent in medically ill patients (Buoli, Caldiroli, &
Altamura, 2016; Buoli, Malerba, Serati, Altamura, & Lanfranconi, 2016; Mago, Gomez,
Gupta, & Kunhel, 2006), including those with renal failure (Oyekçin, Gülpek, Sahin, &
Mete, 2012). Chronic kidney disease (CKD) and chronic renal failure (CRF) are frequent
in the United States and throughout the world, with a prevalence of 13% among adults
(Kittiskulnam, Sheshadri, & Johansen, 2016). Of note, CKD and especially the future
necessity of renal replacement therapy represent a major stress for the affected individu-
als and, consequently, require considerable social adaptation (Kittiskulnam et al., 2016).

CONTACT  M. Buoli  massimiliano.buoli@unimi.it

© 2018 Informa UK Limited, trading as Taylor & Francis Group
2   D. GUENZANI ET AL.

Depression represents the most common psychiatric condition and the second most fre-
quent medical comorbidity after hypertension in these patients (Silva Junior et al., 2014);
its estimated prevalence is 21–27% in non-dialytic patients (Fan et al., 2014) and it might
be even higher in End-Stage Renal Disease (ESRD) patients than in subjects with mild
CKD (Feroze, Martin, Reina-Patton, Kalantar-Zadeh, & Kopple, 2010; Najafi, Keihani,
Bagheri, Ghanbari Jolfaei, & Mazaheri Meybodi, 2016). Depression may worsen overall
medical outcomes of patients with CKD lowering compliance to medications and lifestyle
modifications, and ultimately leading to an increased risk of hospitalization and a faster
deterioration of nutritional status (Fan et al., 2014). In addition, patients with CKD and
depressive symptoms have a poorer quality of life, more functional impairment and higher
mortality compared to subjects without depression (Fan et al., 2014). Suicidal ideation
and attempts (Silva Junior et al., 2014) as well as cognitive impairment (Agganis et al.,
2010) may also contribute to poor outcome of hemodialysis patients with a concomitant
depressive disorder.
Diagnosis of depression in CKD patients is hampered by the fact that mood symp-
toms may mimic the organic manifestations of CRF (fatigue, lethargy, sleep disturbance,
decreased concentration, decreased appetite and decreased libido); on the contrary, several
medications, prescribed to these patients, are associated with side effects which look like
to mood symptoms (Kimmel, 2002).
The etiology of depression in CKD patients is multifactorial with the implication of
biological (increased cytokine levels, genetic predisposition, neurotransmitter dysregu-
lation), psychological (feelings of hopelessness, lack of control) and social factors (loss
of job, poor social networks, social withdrawal, reduced family support) (Pompili et
al., 2013). Of note, several studies found elevated levels of pro-inflammatory cytokines
in mood disorders (Altamura, Buoli, & Pozzoli, 2014), and depressive symptoms have
been observed in patients who received repeated injections of recombinant cytokines
(Pinto & Andrade, 2016). Chronic inflammatory state is common among patients with
advanced CKD; increased levels of cytokines (IL-1, IL-6 and TNF-α) are mainly due to
abnormal clearance of immune mediators, persistent infections, over-hydration and obe-
sity (Taraz, Taraz, & Dashti-Khavidaki, 2015). However, the causal relationship between
inflammation and depressive symptoms in CKD patients need to be further clarified
(Taraz et al., 2015).
Some socio-demographic factors have been associated with depression and suicidal
ideation of patients with CKD, including advanced age and low education status (Keskin
& Engin, 2011). On the other hand, marital status, perceived well-being and social sup-
port all prevent the development of mood symptoms in these patients (Daneker, Kimmel,
Ranich, & Peterson, 2001; Kimmel, 2002). As well as mood disturbances, anxiety disorders
and sexual symptoms are frequent in patients with CKD (about 27–46%) (Pompili et al.,
2013). Sexual dysfunction may be associated with secondary endocrine dysfunctions due
to uremia, antihypertensive medicines, medical (e.g. diabetes) and psychiatric comorbid-
ities (e.g. depressive disorders). Of note, depression is characterized by loss of interest,
reduction in energy, low self-esteem and inability to experience pleasure and these all
conditions cause difficulties in sexual relationship and loss of sexual desire (Fabre & Smith,
2012; Fabre, Clayton, Smith, Goldstein, & Derogatis, 2013). Conversely, sexual dysfunction
can exacerbate depressive symptoms, reducing self-esteem and generating emotional and
marital tension (Oyekçin et al., 2012). Till now very few data have been published about
 PSYCHOLOGY, HEALTH & MEDICINE   3

the presence of psychiatric symptoms in patients with mild CKD. Furthermore, it has not
been still clarified if a more compromised renal function corresponds to a major severity
of psychiatric symptoms. In light of these observations, purpose of the present research
was to study the correlation between severity of renal impairment and deterioration of
mental health.

Methods
We evaluated 100 subjects that were randomly selected among prevalent patients that
attended outpatient clinic of the Department of Nephrology, University of Milan, for at
least 12 months from September 2014 to February 2016. Simple randomization was used
as method of selection. Enrolled subjects had a diagnosis of CKD stages 3 to 5 not yet
in renal replacement therapy and they were followed-up by nephrologists, psychiatrists
and psychologists. We excluded patients that were not able to cooperate, those that were
deemed to have a life expectancy lower than 6 months and those with a previous diagnosis
of primary mood or psychotic disorder according to DSM-5 (Diagnostic and Statistical
Manual for Mental Disorders) (American Psychiatry Association, 2013). All patients were
requested to sign an informed consent before participation to the study in accordance with
Helsinki declaration.
The study was cross-sectional and patients were evaluated through the following
rating scales that were administered by a trained psychologist: Mini-Mental State
Examination (MMSE), Beck Depression Inventory (BDI), Symptom Checklist (SCL-90),
Kidney Disease Quality of Life- Short Form (KDQOL-SF) and Cumulative Illness Rating
Scale (CIRS). MMSE was selected to assess cognitive deterioration, BDI to evaluate
depression severity (Craven, Rodin, & Littlefield, 1988), SCL-90 to assess presence and
severity of psychiatric symptoms, KDQOL-SF to evaluate quality of life (Hays, Kallich,
Mapes, Coons, & Carter, 1994) and CIRS to measure medical comorbidity. KDQOL
was originally thought for patients who underwent dialysis (Hays et al., 1994), however
subsequent researches used this tool, particularly the short form in pre-dialysis patients
with CKD (Hansen, Chin, Blalock, & Joy, 2009; Wee et al., 2016), and it is currently
considered a valid scale to assess quality of life of both pre-dialysis and dialysis CKD
patients (Aiyegbusi et al., 2017).
Collected data included socio-demographic (age, gender, marital status, number of years
of education, presence of a caregiver) and clinical variables (global and sub-item rating
scale scores, presence of medical comorbidity, pharmacological treatment, systolic and
diastolic blood pressure, creatinine, 24-h proteinuria). Glomerular Filtration Rate [eGFR]
was estimated by using CKD EPI formula.
A BDI score ≥12 was considered as pathological (Kjaergaard, Arfwedson Wang, Waterloo,
& Jorde, 2014), while cognitive impairment was defined by a MMSE score ≤24 corrected
for age (An & Liu, 2016).
Descriptive analyses of the total sample were performed. A multiple linear regression
analysis was performed considering eGFR as dependent variable and age, MMSE total
score, BDI total score and the scores of the most significant items of KDQOL-SF (general
health perception, effects of kidney disease on daily life, burden of kidney disease and social
interaction) as independent variables. Linear regression analysis model was weighted for
CIRS severity to attenuate the effect of comorbid medical conditions as confounding factors
4   D. GUENZANI ET AL.

The level of statistical significance was set at p < .05. Statistical Package for Social Sciences
(SPSS) for Windows (version 22.0) was used as statistical analysis program. Sample size was
considered as adequate, hypothesizing a confidence interval of continuous variable of 12
and an original population of 1000 subjects. In this case a sample of 62 patients is sufficient
to have reliable results (Flight & Julious, 2016).

Results
Descriptive analyses on the total sample
The sample included 100 patients: 62 males (62%) and 38 females (38%); the mean age was
77.86 (SD = 6.96) years. Sixty-three per cent of patients were married or had a cohabitant.
Regarding medical history, 99% of patients had high blood pressure, 42% were diabetic
and 55% had suffered from cardio and cerebrovascular events. Thirty-eight and forty per
cent of the total sample presented respectively cognitive impairment (MMSE score ≤24) or
depression (BDI score ≥12). Ten subjects (10%) presented a full-blown major depressive
episode according to DSM-5 criteria. Considering BDI sub-items, suicidal thoughts were
reported by 10% of the total sample and 65% of patients presented loss of sexual interest.
A summary of the results are presented in Table 1.

Multiple linear regression analysis

Multiple linear regression model weighted for CIRS severity was found to be valid (Durbin-
Watson test: 2.2). Age (r = −.13, p = .11), MMSE scores (r = .03, p = .41), BDI scores (r = −.08,
p = .23) and the scores of the items general health perception (r = .02, p = .49) and social
interaction (r = .02, p = .43) of KDQOL-SF did not correlated with eGFR. In contrast a
worse eGFR significantly correlated with the score about the effects of kidney disease on
daily life (r = .25, p = .01) (Figure 1) and the burden of kidney disease (r = .18, p = .05).
Statistical significance of kidney disease on daily life persisted also in the final multivariate
model (t = 2.04, p = .04), differently from the burden of kidney disease (t = 1.20, p = .23).

Discussion
In accordance to what was reported by literature, a high percentage of patients (65%) in
this sample showed loss of sexual interest (Toorians et al., 1997). Furthermore, almost
40% of patients presented depression and cognitive impairment, while 10% had suicidal
ideation. Frequent cognitive impairment in CKD patients was also reported by another
recent research with obvious implications on subjects’ self-care capacity, quality of life and
treatment adherence (Rodríguez-Angarita, Sanabria-Arenas, Vargas-Jaramillo, & Ronderos-
Botero, 2016). Of note, the peculiarity of our results is that, despite the high frequency of
depressive and cognitive symptoms in our sample, these appear to be independent from
the severity of renal illness (Shidler, Peterson, & Kimmel, 1998).
Depression, a potentially modifiable risk factor to improve outcome of subjects with CKD,
is often under-diagnosed because clinicians tend to focus only on physical aspects of the
disease (Bautovich, Katz, Smith, Loo, & Harvey, 2014). Of note, few studies monitored psy-
chiatric symptoms or investigated the frequency of prescription of psychopharmacological
 PSYCHOLOGY, HEALTH & MEDICINE   5

Table 1. Socio-demographic and clinical variables of the total sample.

Total sample
Variables (N = 100)
Gender Male 62 (62.0%)
Female 38 (38.0%)
Age (years) 77.86 (±6.96)
Marital status Single 12 (12.0%)
Married/ cohabitant 63 (63.0%)
Widow/Widower 25 (25.0%)
Years of education 3 3 (3.0%)
4 1 (1.0%)
5 19 (19.0%)
6 2 (2.0%)
7 1 (1.0%)
8 16 (16.0%)
10 2 (2.0%)
11 8 (8.0%)
12 2 (2.0%)
13 28 (28.0%)
18 18 (18.0%)
Caregiver No 24 (24.0%)
Yes 76 (76.0%)
MMSE total score 24.75 (±2.86)
Pat MMSE No 62 (62.0%)
Yes 38 (38.0%)
BDI-II total score 10.74 (±7.32)
Pat BDI No 60 (60.0%)
Yes 40 (40.0%)
Suicidal thoughts (BDI) No 90 (90.0%)
  Yes 10 (10.0%)
Loss of sexual interest (BDI) No 35 (35%)
Yes 65 (65%)
Pat SCL-90 Somatization No 81 (81.0%)
Yes 19 (19.0%)
Obsessive-Compulsive No 92 (92.0%)
Yes 8 (8.0%)
Interpersonal Sensitivity No 93 (93.0%)
Yes 7 (7.0%)
Depression No 90 (90.0%)
Yes 10 (10.0%)
Anxiety No 94 (94.0%)
Yes 6 (6.0%)
Hostility No 97 (97.0%)
Yes 3 (3.0%)
Phobic Anxiety No 89 (89.0%)
Yes 11 (11.0%)
Paranoid Ideation No 96 (96.0%)
Yes 4 (4.0%)
Psychoticism No 93 (93.0%)
Yes 7 (7.0%)
Global Severity Index No 93 (93.0%)
Yes 7 (7.0%)
Hypertension No 1 (1.0%)
Yes 99 (99.0%)
Diabetes No 58 (58.0%)
Yes 42 (42.0%)
Cerebrovascular events No 45 (45.0%)
Yes 55 (55.0%)
ACE-i/ARB No 48 (48.0%)
ARB 34 (34.0%)
ACE-i 16 (16.0%)
Both 2 (2.0%)
Diuretics No 31 (31.0%)
Yes 69 (69%)
(Continued)
6   D. GUENZANI ET AL.

Table 1. (Continued).
Total sample
Variables (N = 100)
Psychiatric treatment No 78 (78.0%)
Anxiolytics 14 (14.0%)
Antidepressants 6 (6.0%)
Both 2 (2.0%)
KDQOL General Health Perception 81.54 (±13.00)
Effects of Kidney Disease on Daily Life 84.44 (±13.24)
Burden of Kidney Disease 64.41 (±24.65)
Quality of Social Interaction 78.75 (±18.41)
Systolic blood pressure (mmHg) 137.85 (±17.93)
Diastolic blood pressure (mmHg) 77.44 (±11.57)
Creatinine (mg/dl) 2.35 (±.96)
Proteinuria 24 h (mg) 718.32 (±1007.51)
CIRS severity 2.02 (±0.26)
CIRS comorbidity 4.34 (±1.70)
eGFR >26 50 (50.0%)
≤26 50 (50.0%)
Notes: Standard deviations are reported into brackets.
Legend:
ACE-i: ACE inhibitors.
ARB: Angiotensin Receptor Blockers.
BDI: Beck Depression Inventory.
CIRS: Cumulative Illness Rating Scale.
eGFR: estimated glomerular filtration rate.
KDQOL-SF: Kidney Disease Quality of Life Instrument (KDQOL).
MMSE: Mini Mental State Examination.
Pat: Pathological.
SCL-90: The Symptom Checklist-90.

Figure 1. Effects of kidney disease on daily life in relation to glomerular filtration rate.
 PSYCHOLOGY, HEALTH & MEDICINE   7

treatments in CKD patients (Bautovich et al., 2014). Given the effects on quality of life and
medical outcome, clinicians should early recognize depression, anxiety or other psychiatric
symptoms during follow-up of subjects with CRF (Dell’Osso, Camuri, Benatti, Buoli, &
Altamura, 2013). Of note, a multidisciplinary approach, involving nephrologists, psychi-
atrists and psychologists, should become part of routine evaluation of CKD patients in
conservative therapy (Even & Grunfeld, 2008). On the other hand, treatment of depression
in CKD patients requires specific expertise: many antidepressants may impact on renal
function so that under-treatment of depression and under-dosing of antidepressants may
be the consequence of clinicians’ concern about adverse effects of pharmacotherapy (Buoli,
Mauri, & Altamura, 2014).
As mentioned above, another remarkable issue in CKD is the high prevalence of cognitive
impairment (Rodríguez-Angarita et al., 2016). Consequently, periodic cognitive assessment
should become a common practice in nephrology outpatient clinics. Early identification of a
cognitive impairment could help to treat possible modifiable factors of mental deterioration.
Furthermore, cognitive impairment impacts on patients’ compliance to treatment thus it
should be recognized in order to individualize the educational and therapeutic program of
patients with CKD. Of note, it is already known that patients with cognitive impairment are
particularly frail and incur in a faster decline of renal function (Chan et al., 2011).
In contrast, our study showed that few psychiatric outcomes are correlated with severity
of renal dysfunction, particularly those related to quality of life and daily functioning. Of
note the most statistically significant sub-item of KDQOL-SF (effects of kidney disease on
daily life) refers to the limits due to diet restriction and the feelings of dependent on doctors.
These findings might be explained on the basis of the unrelenting, long-term nature of
the disease and the intensity and duration of its treatment, but also on the anxiety derived
from the necessity to start a renal replacement therapy in the near future (Rahimipour,
Shahgholian, & Yazdani, 2015). In particular, the idea of the forthcoming dialysis may
induce the patients to develop strong concerns about the future psychological and physical
dependence from the technique of renal replacement therapy (Rahimipour et al., 2015).
Taken overall, our data indicate that depressive symptoms (including loss of sexual inter-
est) would be more related to chronic disease diagnosis itself (Charova, Dorstyn, Tully, &
Mittag, 2015), while a major severity of illness would result in increased stress tied to the
near loss of autonomy associated with the commencement of renal replacement therapy.
Some limitations of the present study should be shortly described. First, this is a cross-sec-
tional naturalistic study that has the advantage to be adherent to clinical practice, but the
disadvantage to potentially include confounding factors in the analyses. We tried to limit
the influence of confounding factors in the results, weighting our analyses with CIRS sever-
ity scores. Another limitation is represented by questionnaires such as KDQOL-SF which
cannot be as accurate as those used to assess severity of primary psychiatric disorders.
Furthermore, as mentioned above, KDQOL was originally thought for patients in dialy-
sis, however this tool is currently considered as reliable also for pre-dialysis patients with
CKD (Aiyegbusi et al., 2017). Finally, the reported correlations between severity of renal
dysfunction and quality of life/daily functioning are weak and need to be confirmed by
future large-sample prospective studies. The strengths of this study are represented by the
stratification for age and comorbidity index, and by randomization with the aim to restitute
a reliable picture of the prevalence and severity of psychiatric and cognitive impairment in
a prevalent cohort of patients with a mild to severe CKD.
8   D. GUENZANI ET AL.

Disclosure statement
The authors declare no conflict of interest.

ORCID
M. Buoli   http://orcid.org/0000-0003-3359-3191

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