Clin. Lab.

2023;69:92-98
©Copyright
ORIGINAL ARTICLE

The Relationship between Zonulin and Metabolic Syndrome in

Renal Transplant Patients
Gulbanu Canbaloglu Erkan 1, Abdullah Sumnu 2, Gokhan Ertugrul 3, Gozde Ulfer 4, Cagri Cakici 4,
Huseyin Cagatay Aydin 3, Aydin Unal 2
1
Istanbul Medipol University, Faculty of Medicine, Department of Gastroenterology, Istanbul, Turkey
2
Istanbul Medipol University, Faculty of Medicine, Department of Nephrology, Istanbul, Turkey
3
Istanbul Medipol University, Faculty of Medicine, Department of Surgery, Organ Transplantation Center, Istanbul, Turkey
4
Istanbul Medipol University, Faculty of Medicine, Department of Biochemistry, Istanbul, Turkey

SUMMARY

Background: Levels of zonulin, a surrogate marker of intestinal permeability, are elevated in various disorders in-
cluding insulin resistance, obesity, celiac disease, and inflammatory bowel disease. We aimed to elucidate the asso-
ciation of zonulin levels and metabolic syndrome (MS) in renal transplant recipients.
Methods: Seventy-nine renal transplant recipients were enrolled. Diagnosis of MS was established employing the
Adult Treatment Panel III (ATP III) criteria. Serum zonulin level was determined using the double antibody
sandwich ELISA method.
Results: MS was encountered in 37 (41.6%) of the 79 patients. Serum zonulin level was significantly higher in pa-
tients with MS compared to those without MS (p < 0.001). Serum zonulin level correlated with presence of MS (r:
739, p < 0.001), abdominal obesity (r: 514, p < 0.001), fasting glucose level (r: 361, p: 0.001), presence of fasting
glucose/diabetes criterion of MS (r: 316, p: 0.005), presence of low HDL criterion of MS (r: 266, p: 0.018), and
BMI (r: 527, p < 0.001).
Conclusions: A Zonulin-mediated increase in intestinal permeability may play a role in the pathogenesis of meta-
bolic syndrome. We propose that zonulin may be a suitable surrogate marker of MS in renal transplant recipients.
(Clin. Lab. 2023;69:92-98. DOI: 10.7754/Clin.Lab.2022.220341)

Correspondence: KEYWORDS
Gulbanu Canbaloglu Erkan, MD
Medipol Mega Universite Hastanesi zonulin, kidney transplantation, metabolic syndrome,
TEM Avrupa Otoyolu Goztepe Cikisi No. 1 body mass index, glucose
Bagcilar, Istanbul
Turkey
Phone: +90 (212) 4607777
Fax: +90 (212) 4607070 INTRODUCTION
Email: gcanbaloglu@yahoo.com
Metabolic syndrome (MS) comprises traditional risk
factors for atherosclerosis, including impaired glucose
tolerance, hypertension, abdominal obesity, and dyslip-
idemia [1]. While the exact pathophysiology of MS is
not clear, insulin resistance is thought to play a crucial
role in its progression [2]. The combination of excess
calorie intake and a sedentary lifestyle leads to weight
gain and alterations in adipose tissue metabolism, which
promote insulin resistance (IR) [3]. IR causes vascular
_______________________________________________________ endothelial dysfunction and vascular wall inflammation,
Manuscript accepted April 24, 2022 which in turn pave the way for atherosclerosis.

92 Clin. Lab. 1/2023

 G. C. Erkan et al.
MS is an important concern in renal transplant recipi-
ents, as it is a major determinant of graft failure and car-
diovascular events [4,5]. It is well-known that MS is
more common in renal transplant recipients than in the
population at large [6]. The preponderance of MS in this
patient population may be explained by the frequent and
mandatory use of immunosuppressive drugs such as
corticosteroids and tacrolimus [7,8].
Zonulin, a 47-kDa protein synthesized mainly in the liv-
er and similar in structure to prehaptoglobin-2, regulates
intestinal permeability by binding to the epidermal
growth factor receptor (EGFR) and protease activated
receptor-2 (PAR-2) [9]. Elevated serum zonulin levels
reflect impairment of the intestinal barrier function [10].
Serum zonulin concentrations are also higher in obese
and/or diabetic subjects [11,12]. Zonulin levels are also
elevated in diarrhea predominant irritable bowel syn-
drome [13], inflammatory bowel disease [14] and celiac
disease [15]. Studies published so far about zonulin lev-
els in chronic kidney disease are somewhat controver-
sial. Ficek et al. [16] reported serum zonulin concentra-
tions to be higher in hemodialysis patients than those in
healthy controls, whereas Lukaszyk [17] et al. found
zonulin concentrations to be lower than in healthy con-
trols.
Serum levels of zonulin are increased in association
with obesity-related insulin resistance, and it has been
proposed that this association may be mediated by obe-
sity-related increase in IL-6 levels [18]. A recent study
found that gut permeability, which is known to be regu-
lated by zonulin, might have a distinctive role in IR in
healthy obese young adults [19]. The same study also
reported that zonulin positively correlated with HOMA-
IR and insulin levels.
Our purpose was to elucidate the prevalence of MS and
the serum levels of zonulin, the levels of which are as-
sociated with components of MS, in renal transplant re-
cipients.
MATERIALS AND METHODS
This cross-sectional study comprised 79 adult renal
transplant recipients from our outpatient transplant clin-
ic. The inclusion criteria consisted of age above 18
years, duration after transplantation of at least six
months, and stable graft function (serum creatinine level
< 2 mg/dL) in the preceding 3 months. Biochemistry
findings and anthropometric measurements (weight,
height, and waist circumference) were retrieved from
the patients' medical records. Demographic data, the un-
derlying cause of end-stage renal disease (ESRD), anti-
hypertensive medications, anti-lipidemic drugs, immu-
nosuppressive agents, and post-transplant duration were
noted. Body mass index (BMI) was calculated as weight
in kilograms divided by height in meters squared (kg/
m2). Waist circumference (WC) was measured at the
mid-point between the lower border of the arcus costar-
ium and the crista iliaca.
Clin. Lab. 1/2023
The diagnosis of MS was established using the updated
Adult Treatment Panel III (ATP III) criteria. MS was di-
agnosed upon the detection of any 3 of the five criteria:
(1) abdominal obesity, denoted by WC ≥ 102 cm in men
and ≥ 88 cm in women, (2) serum triglycerides ≥ 150
mg/dL or being on triglyceride lowering therapy, (3) se-
rum high-density lipoprotein (HDL) cholesterol < 40
mg/dL in men and < 50 mg/dL in women or being on
medical therapy to raise HDL cholesterol levels, (4)
≥ 130 mmHg systolic blood pressure or ≥ 85 mmHg
diastolic blood pressure or current antihypertensive drug
therapy, (5) fasting plasma glucose ≥ 100 mg/dL or
medical therapy for elevated blood glucose [1].
For the detection of serum zonulin level, 10 mL of
blood was obtained from all subjects after 12 hours of
fasting. After coagulation for 10 - 20 minutes, the sam-
ples were centrifuged at 3,000 rpm for 20 minutes. The
separated serum was stored at -80℃. Serum zonulin
concentration was determined using a human zonulin
enzyme-linked immunosorbent assay (ELISA) kit
(Sunred Biological Technology Company, Shanghai,
China). Zonulin concentration was determined with the
double antibody sandwich ELISA method. The detec-
tion range of the kit was 0.25 - 70 ng/mL, and the lower
limit of detection was 8 ng/mL.
Written informed consent was obtained from all sub-
jects for participation in the study, which had already
been approved by the Ethical Review Board of our in-
stitution (Approval date: 25.07.2018, Approval number:
423).
Statistical analysis
Statistical analysis was calculated using SPSS 22.0. The
Shapiro-Wilk test was employed to assess the normality
of distribution of numerical variables. Variables that
displayed normal distribution were presented as mean
values + standard deviations. Median values were used
when normal distribution was not observed. Analysis
for the parametric variables was carried out with Stu-
dent’s t-test between two groups. The Mann-Whitney U
test was used to compare nonparametric variables be-
tween two groups. The correlation analysis was carried
out using Spearman’s correlation test. Categorical vari-
ables are presented as percent and the χ2 test was used
to evaluate the correlation between the categorical vari-
ables. Statistical analysis for the parametric variables
was carried out using one-way ANOVA with Scheffe's
post-hoc test among three groups. A p-value < 0.05 was
considered to be statistically significant.
RESULTS
The mean age of the 79 patients was 43.0 ± 14.1 years;
27 (34.2%) of the 79 patients were female. Mean serum
creatinine level was 1.2 ± 0.3 mg/dL. MS was found in
37 (41.6%) of the 79 patients with renal transplantation.
The underlying cause of ESRD was glomerulonephritis
in 21 (26.6%), diabetes mellitus in 15 (19.0%), hyper-
93
 Zonulin and Metabolic Syndrome in Renal Transplant Patients

Table 1. Comparison of demographic, clinical, and laboratory parameters between renal transplant patients with and without
MS.

Patients with MS Patients without MS

p-value
(n: 37) (n: 42)
Age (year) 49.4 ± 12.1 37.4 ± 13.4 < 0.001
Female/Male (%) 18 (48.6)/19 (51.4) 9 (21.4)/33 (78.6) 0.017
Type of donor (living/cadaveric) (%) 33 (89.2)/4 (10.8) 39 (92.9)/3 (7.1) 0.700
Serum zonulin level (ng/mL) 18.3 ± 2.4 13.4 ± 2.4 < 0.001
Post-transplant duration (month) 13 (7 - 48) 8 (7 - 41) 0.400
BMI (kg/m2) 30.9 (21.1 - 41.5) 24.5 (16.9 - 33.8) < 0.001
BMI classification < 0.001
Underweight (< 18.5 kg/m2) (%) - -
Healthy weight (18.5 - 24.9 kg/m2) (%) 5 (13.5) 27 (64.3)
Overweight (25.0 - 29.9 kg/m2) (%) 12 (32.4) 13 (31.0)
Obese (≥ 30.0 kg/m2) (%) 20 (54.1) 2 (4.8)
Waist circumference (cm) 110 (78 - 128) 93 (70 - 117) < 0.001
Systolic blood pressure (mmHg) 120.8 ± 20.5 125.5 ± 16.1 0.261
Diastolic blood pressure (mmHg) 70.5 ± 8.5 72.6 ± 8.0 0.265
Serum creatinine (mg/dL) 1.16 ± 0.34 1.23 ± 0.28 0.341
Total cholesterol level (mg/dL) 214 ± 60 184 ± 43 0.014
Triglyceride level (mg/dL) 204 (70 - 743) 129 (55 - 902) 0.002
High-density lipoprotein level (mg/dL) 48 (30 - 103) 57 (29 - 110) 0.005
Low-density lipoprotein level (mg/dL) 118 ± 55 96 ± 32 0.033
Fasting serum glucose level (mg/dL) 110 (67 - 971) 93 (70 - 944) 0.001
Proteinuria (mg/day) 182 (9 - 2,266) 123 (70 - 604) 0.157
Serum albumin (g/dL) 4.2 ± 0.3 4.3 ± 0.3 0.140
Serum uric acid 5.8 ± 1.6 6.3 ± 1.6 0.146
Use of immunosuppressive agent 0.087
Tacrolimus (%) 41 (97.6) 31 (83.8)
Everolimus (%) 1 (2.4) 4 (10.8)
Cyclosporine (%) - 2 (5.4)

tension in 3 (3.8%), vesicoureteral reflux (VUR) ne-
phropathy in 3 (3.8%), kidney stone disease in 2 (2.5%),
other causes 6 (7.6%), and unknown in 29 (36.7%) pa-
tients.
All patients except one patient, who had used tacroli-
mus + everolimus + prednisolone, received the follow-
ing immunosuppressive protocol; a calcineurin inhibitor
(tacrolimus/cyclosporine) or everolimus + mycopheno-
late mofetil/mycophenolic acid + corticosteroid (pred-
nisolone 5 mg/day or methylprednisolone 4 mg/day).
Table 1 shows comparison of clinical, demographic,
and laboratory parameters between renal transplant pa-
tients with and without MS. Serum zonulin concentra-
tion was significantly elevated in subjects with MS
compared to those without MS (18.3 ± 2.4 vs. 13.4 ±
2.4 ng/mL, p < 0.001). Figure 1 shows serum zonulin
levels in both groups.
Age, BMI, WC, total cholesterol, triglyceride, low-den-
sity lipoprotein (LDL)-cholesterol levels, and fasting
glucose were significantly higher in patients with MS
compared to those without MS (p < 0.001, < 0.001,
< 0.001, < 0.014, < 0.002, < 0.033, and < 0.001; respec-
tively). High-density lipoprotein (HDL)-cholesterol lev-
el was significantly lower in patients with MS compared
to those without MS (p < 0.005). There was a signifi-
cant difference between the groups in terms of gender
and BMI classification. Male gender was predominant
in patients without MS whereas the proportions of both
genders were similar in patients with MS (p < 0.017).
More than half of patients with MS were obese whereas
most of the patients without MS had a healthy weight
(p < 0.001).
Comparison of serum zonulin concentrations in groups
defined according to components of MS, BMI, and gen-

94 Clin. Lab. 1/2023

 G. C. Erkan et al.

Table 2. Comparison of serum zonulin levels in patient groups classified according to components of MS, BMI, and gender.

Serum zonulin level (ng/mL) p-value

Gender 0.089
Female 16.6 ± 3.2
Male 15.2 ± 3.4
Abdominal obesity < 0.001
Presence 17.4 ± 3.1
Absence 13.9 ± 2.8
Blood pressure/hypertension criteria of MS 0.152
Presence 16.0 ± 3.5
Absence 14.6 ± 2.6
Fasting glucose/diabetes criteria of MS 0.011
Presence 17.4 ± 2.9
Absence 15.1 ± 3.4
Hypertriglyceridemia criteria of MS 0.393
Presence 16.0 ± 3.4
Absence 15.3 ± 3.5
Low HDL criteria of MS 0.060
Presence 16.9 ± 2.7
Absence 15.2 ± 3.6
BMI classification * < 0.001
Healthy weight (18.5 - 24.9 kg/m2) 14.0 ± 2.8
Overweight (25.0 - 29.9 kg/m2) 15.5 ± 3.3
Obese (≥ 30.0 kg/m2) 18.4 ± 2.7

Figure 1. Comparison of serum zonulin level between patients with and without metabolic syndrome.

Clin. Lab. 1/2023 95

 Zonulin and Metabolic Syndrome in Renal Transplant Patients
der are presented in Table 2. Serum zonulin concentra-
tion was significantly elevated in patients with abdomi-
nal obesity compared to those without (p < 0.001). It
was significantly higher in patients, who had fasting
glucose/diabetes criterion of MS, compared to those
without this criterion (p < 0.011). There was a signifi-
cant difference among BMI classification groups with
regard to serum zonulin concentration (p < 0.001). It
was significantly higher in the obese group compared to
the other groups; however, there was no significant dif-
ference between the healthy weight group and the over-
weight group.
Serum zonulin level correlated with age (r < 0.473, p <
0.001), WC (r < 0.528, p < 0.001), presence of MS (r <
739, p < 0.001), abdominal obesity (r < 514, p < 0.001),
fasting glucose level (r < 361, p < 0.001), presence of
fasting glucose/diabetes criterion of MS (r < 316, p <
0.005), presence of low HDL criterion of MS (r < 266,
p < 0.018), and BMI (r < 527, p < 0.001).
DISCUSSION
MS was found in 37 (41.6%) of the 79 renal transplant
patients in our cohort. Comparable prevalence has been
reported in other studies. Fabbian et al. have found that
37 (34.5%) of 107 stable Italian renal transplant patients
had MS [20]. The prevalence of MS has been observed
to be 32% in 121 Chinese renal transplant recipients [6].
Another study conducted on 106 stable Iranian renal
transplant recipients reported that 52.8% of this patient
group had MS [21]. Recently, the prevalence of MS has
been observed to be 62.6% in 155 Turkish renal trans-
plant recipients [22]. Post-transplant MS is not confined
to renal transplantation, the prevalence of MS in liver
transplant recipients has been reported to be in the range
of 44% to 58%, and is associated with adverse cardio-
vascular outcomes [23].
The incidence of MS also seems to further increase after
renal transplantation. In a study by Porrini et al. [5],
among 230 renal cadaveric transplant recipients with
stable graft function at 1 year (baseline), the incidence
of MS was 22.6%. This relatively high incidence (when
compared to the population at large) at baseline may be
attributed to the fact that almost all components of the
MS (i.e., obesity, hyperglycemia, dyslipidemia) are also
risk factors for developing chronic kidney disease. The
incidence of MS rose to 36.6 percent at 18 months from
baseline evaluation. This increase may be explained by
the use of immunosuppressive medications such as cor-
ticosteroids and tacrolimus, which are known to inter-
fere with glucose metabolism.
Immunosuppressive drugs such as corticosteroids, calci-
neurin inhibitors, and mammalian target of rapamycin
(mTOR) inhibitors have deleterious effects on compo-
nents of the MS at post-transplant period. Corticoste-
roids may bring about increased appetite and thus may
cause weight gain, which may be prominent in some pa-
tients. Glucocorticoids bring about decreased glucose
96
tolerance, sensitivity to insulin, and increase gluconeo-
genesis. As a result, blood glucose is elevated by 10 -
20% [7]. They may trigger hypertension via several
pathophysiological mechanisms which include in-
creased plasma volume, peripheral vascular resistance,
and cardiac output [24].
IR is the crucial feature of the MS, and its key deter-
minant is the severity of obesity, in particular visceral
obesity [25]. Glucocorticoids exert chronic effects to
promote central obesity and acute effects to accelerate
lipolysis. It is plausible that glucocorticoid excess might
contribute to the abnormalities of free fatty acid metab-
olism in MS [26]. A recent meta-analysis showed that
the incidence of hypertension, new onset diabetes, and
hypercholesterolemia was lowered significantly by ste-
roid avoidance or withdrawal (SAW) regimens, at the
cost of increased risk of acute rejection [27]. Calcineu-
rin inhibitors can trigger hyperlipidemia, hypertension,
and glucose intolerance. mTOR inhibitors may cause
dose-dependent hypertriglyceridemia [8]. In the present
study, almost all patients received an immunosuppres-
sive regimen consisting of a calcineurin inhibitor or an
mTOR inhibitor, mycophenolate, and a corticosteroid.
All patients in our cohort except one had received cor-
ticosteroids. Possibly, immunosuppressive medications
might be one of the leading factors contributing to high
prevalence of MS in our patient cohort.
Serum zonulin concentrations are also elevated in obese
and/or diabetic subjects [11,12]. Reports on serum zon-
ulin concentrations in chronic kidney disease are some-
what conflicting; while one study reported serum zonu-
lin concentrations to be lower in chronic kidney disease
patients than those in healthy controls, in another study
serum zonulin concentrations were found to be higher in
chronic kidney disease patients than those in healthy
controls [16,17]. These contradicting findings warrant
further research and need to be validated in larger scale
studies. To the best of our knowledge, there is one pub-
lished report on serum zonulin levels in renal transplant
recipients. Malyszko et al. found serum zonulin levels
in renal transplant recipients to be lower than those in
healthy controls, nevertheless, the MS status in this co-
hort was not delineated [28]. To the best of our knowl-
edge, there is no published study that has investigated
the relationship between serum zonulin levels and MS
in renal transplant recipients.
In line with previous findings, serum zonulin level was
significantly higher in renal transplant recipients with
MS when compared to those without MS. When the
analysis was further detailed according to individual
components of the MS, renal transplant recipients with
abdominal obesity had higher serum zonulin levels
compared to those without abdominal obesity in our
study. It was also significantly higher in patients who
had fasting glucose/diabetes criterion of MS compared
to those without this criterion. There was a significant
difference among BMI classification groups with regard
to serum zonulin concentration. It was significantly
higher in the obese group compared to both groups but
Clin. Lab. 1/2023
 G. C. Erkan et al.
there was no significant difference between the healthy
weight group and the overweight group. To the best of
our knowledge, this is the first study investigating the
relationship between serum zonulin levels and MS in re-
nal transplant recipients.
Limitations:
The major limitation of our study is the relatively small
sample size.
CONCLUSION
Serum zonulin concentration was significantly higher in
renal transplant recipients with MS when compared to
those without MS. It was significantly higher in patients
with abdominal obesity compared to those without ab-
dominal obesity. It was significantly higher in patients
who had fasting glucose/diabetes criterion of MS com-
pared to those without this criterion. We propose that
zonulin may be a suitable surrogate marker of MS in re-
nal transplant recipients. Zonulin mediated increase in
intestinal permeability may play a role in the pathogene-
sis of metabolic syndrome. This is a pilot study the find-
ings of which warrant further investigation of this sub-
ject.
Acknowledgment:
This study was supported by the Turkish Society of Ne-
phrology (they provided the Zonulin test kits). We
would like to thank the Turkish Society of Nephrology
for their unconditional support.
Statement of Ethics:
Written informed consent was obtained from all sub-
jects for participation in the study, which had already
been approved by the Ethical Review Board of our in-
stitution (Approval date: 25.07.2018, Approval number:
423).
Declaration of Interest:
None.
References:
1. Grundy SM, Cleeman JI, Daniels SR, et al. Diagnosis and man-
agement of the metabolic syndrome. an American Heart Asso-
ciation/National Heart, Lung, and Blood Institute Scientific State-
ment. Circulation 2005;112(17):2735-52. (PMID: 16157765)
2. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome.
Lancet 2005;36:1415-28. (PMID: 15836891)
3. Koh KK, Han SH, Quon MJ. Inflammatory markers and the me-
tabolic syndrome: Insights from therapeutic interventions. J Am
Coll Cardiol 2005;46:1978-85. (PMID: 16325028)
Clin. Lab. 1/2023
4. Goldsmith D, Pietrangeli CE. The metabolic syndrome following
kidney transplantation. Kidney Int Suppl 2010;78 Suppl 118:S8-
14. (PMID: 20706225)
5. Porrini E, Delgado P, Torres A. Metabolic syndrome, insulin re-
sistance, and chronic allograft dysfunction. Kidney Int Suppl
2010;119:S42-6. (PMID: 21116317)
6. Cheung CY, Chan HW, Liu YL, et al. Prevalence of metabolic
syndrome in Chinese renal transplant recipients. Hong Kong Med
J 2008;14:379-84. (PMID: 18840909)
7. Stanbury RM, Graham EM. Systemic corticosteroid therapy--side
effects and their management. Br J Ophthalmol 1998;82:704-8.
(PMID: 9797677)
8. Womer K, Rabb H. Immunosuppressive medications in kidney
transplantation. In: Floege J, Johnson RJ, and Feehally J, editors.
Comprehensive clinical nephrology. 4th edition. Missouri: Else-
vier Saunders 2010. p. 1134-41.
9. Tripathi A, Lammers KM, Goldblum S, et al. Identification of hu-
man zonulin, a physiological modulator of tight junctions, as pre-
haptoglobin-2. Proc Natl Acad Sci USA 2009;106:16799-804.
(PMID: 19805376)
10. Fasano A. Intestinal permeability and its regulation by zonulin:
Diagnostic and therapeutic implications. Clin Gastroenterol Hep-
atol 2012 Oct;10(10):1096-100. (PMID: 22902773)
11. Zak-Golab A, Kocelak P, Aptekorz M, et al. Gut microbiota, mi-
croinflammation, metabolic profile, and zonulin concentration in
obese and normal weight subjects. Int J Endocrinol 2013;2013:
674106. (PMID: 23970898)
12. Zhang D, Zhang L, Zheng Y, Yue F, Russell RD, Zeng Y. Circu-
lating zonulin levels in newly diagnosed Chinese type 2 diabetes
patients. Diabetes Res Clin Pract 2014;106:312-8.
(PMID: 25238913)
13. Linsalata M, Riezzo G, D'Attoma B, Clemente C, Orlando A,
Russo F. Noninvasive biomarkers of gut barrier function identify
two subtypes of patients suffering from diarrhoea predominant-
IBS: a case-control study BMC Gastroenterol 2018 Nov 6;18(1):
167. (PMID: 30400824)
14. Caviglia GP, Dughera F, Ribaldone DG, et al. Serum zonulin in
patients with inflammatory bowel disease: a pilot study. Minerva
Med 2019 Apr;110(2):95-100. (PMID: 30160088)
15. Vojdani A, Vojdani E, Kharrazian D. Fluctuation of zonulin lev-
els in blood vs. stability of antibodies World J Gastroenterol 2017
Aug 21;23(31):5669-79. (PMID: 28883692)
16. Ficek J, Wyskida K, Ficek R, et al. Relationship between plasma
levels of zonulin, bacterial lipopolysaccharides, D-lactate and
markers of inflammation in haemodialysis patients. Int Urol Ne-
phrol 2017 Apr;49(4):717-25. (PMID: 28044237)
17. Lukaszyk E, Lukaszyk M, Koc-Zorawska E, Bodzenta-Lukaszyk
A, Malyszko J. Zonulin, inflammation and iron status in patients
with early stages of chronic kidney disease. Int Urol Nephrol
2018 Jan;50(1):121-5. (PMID: 29134616)
18. Moreno-Navarrete JM, Sabater M, Ortega F, Ricart W, Fernan-
dez-Real JM. Circulating zonulin, a marker of intestinal perme-
ability, is increased in association with obesity-associated insulin
resistance. PLoS One 2012;7(5):e37160. (PMID: 22629362)
19. Mkumbuzi L, Mfengu MMO, Engwa GA, Sewani-Rusike CR. In-
sulin Resistance is Associated with Gut Permeability Without the
Direct Influence of Obesity in Young Adults. Diabetes Metab
Syndr Obes 2020 Aug 24;13:2997-3008. (PMID: 32922055)
97
 Zonulin and Metabolic Syndrome in Renal Transplant Patients

20. Fabbian F, Bergami M, Molino C, et al. Risk factors for metabol-

ic syndrome in stable Italian renal transplant patients. Clin Exp
Nephrol 2011;15:560-6. (PMID: 21360023)

21. Hami M, Sabbagh MG, Sefidgaran A, Mojahedi MJ. Prevalence

of the metabolic syndrome in kidney transplant recipients: A sin-
gle-center study. Saudi J Kidney Dis Transpl 2017 Mar - Apr;
28(2):362-7. (PMID: 28352021)

22. Ecder SA, Sasak G. Body Shape Index Predicts Metabolic Syn-
drome and Insulin Resistance in Renal Transplant Recipients.
Transplant Proc 2019 Sep;51(7):2334-8. (PMID: 31402244)

23. Davis BC, Shadab Siddiqui M. Liver Transplantation: the Role of

Metabolic Syndrome. Curr Treat Options Gastroenterol 2017 Jun;
15(2):316-31. (PMID: 28432575)

24. Magiakou MA, Smyrnaki P, Chrousos GP. Hypertension in

Cushing's syndrome. Best Pract Res Clin Endocrinol Metab 2006;
20:467-82. (PMID: 16980206)

25. Despres JP. Abdominal obesity as important component of insu-

lin-resistance syndrome. Nutrition 1993;9:452-9.
(PMID: 8286886)

26. Macfarlane DP, Forbes S, Walker BR. Glucocorticoids and fatty

acid metabolism in humans. fuelling fat redistribution in the me-
tabolic syndrome. J Endocrinol 2008;197:189-204.
(PMID: 18434349)

27. Knight SR, Morris PJ. Steroid avoidance or withdrawal after re-
nal transplantation increases the risk of acute rejection but de-
creases cardiovascular risk. A meta-analysis. Transplantation
2010;89:1-14. (PMID: 20061913)

28. Malyszko J, Koc-Zorawska E, Levin-Iaina N, Malyszko J. Zonu-

lin, iron status, and anemia in kidney transplant recipients: are
they related? Transplant Proc 2014 Oct;46(8):2644-6.
(PMID: 25380885)

98 Clin. Lab. 1/2023