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Reverse epidemiology in peritoneal dialysis patients: The Canadian

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Int Urol Nephrol (2007) 39:281–288
DOI 10.1007/s11255-006-9142-1
ORIGINAL PAPER
Reverse epidemiology in peritoneal dialysis patients:
the Canadian experience and review of the literature
T. Pliakogiannis Æ L. Trpeski Æ H. Taskapan Æ
H. Shah Æ M. Ahmad Æ S. Fenton Æ J. Bargman Æ
D. Oreopoulos
Received: 20 August 2006 / Accepted: 22 October 2006 / Published online: 14 December 2006

Springer Science+Business Media B.V 2006
Abstract High Body Mass Index (BMI) has
been associated with improved survival of End-
Stage Renal Disease (ESRD) patients on chronic
hemodialysis (HD); however, studies on the
relationship of BMI with survival in Peritoneal
Dialysis (PD) patients have yielded conflicting
results. The purpose of this study was to evaluate
the impact of BMI on survival of Canadian ESRD
patients on PD, correcting for their age, sex, race,
diabetes mellitus, and arterial hypertension. In an
intent to treat study, we reviewed data of the
Canadian Organ Replacement Register (CORR),
of incident patients, starting PD between 1994
and 1998 and followed up from their initial PD
treatment to the end of 2003. Patients were
censored at loss to follow up, transplantation,
and the end of the observation period. Cox
regression (multivariate) analysis was performed
and adjustments were made for age, gender, race,
primary renal disease and BMI. During these
years, 4054 patients commenced PD, 1742 (43%)
of them were females and 1471 (36.3%) were
T. Pliakogiannis (&)
H. Taskapan
H. Shah

M. Ahmad
S. Fenton
J. Bargman
D. Oreopoulos
University Health Network, University of Toronto,
Toronto, Ontario, Canada
e-mail: teopliakogiannis@yahoo.ca
L. Trpeski
Canadian Organ Replacement Register, Canadian
Institute of Health Information, Toronto, Canada
diabetics. The majority were Caucasians (n=3058,
75.4%); 120 (3%) belonged to the First Nations,
137 (3.4%) were black, and the rest
(739 pts—18.2%) belonged to various other eth-
nicities. Based on quartiles of the BMI distribu-
tion, 1130 patients (28%) had a BMI < 18.5 kg/
m2; 1163 (28.7%), 18.5–24.9 kg/m2; 1214 (30%),
25–29.9 kg/m2; 547 (13.5%) > 30 kg/m2. Intent to
treat Cox regression analysis showed that being
underweight was a strong risk factor for death.
Specifically, a BMI less than 18.5 was associated
with a death hazard ratio (HR) 1.3, (CI: 1.1–1.6).
On the contrary, BMI > 30 was not associated
with worse survival than those with normal BMI
(HR = 1.009, CI = 0.89–1.14). High-BMI patients
should not be discouraged from PD just because
of their size.
Keywords Body mass index

Peritoneal dialysis
Reverse epidemiology
Introduction
In most developed countries, the prevalence of
obesity is increasing. A recent Canadian report
indicated that 15% of the Canadian population
aged between 20 and 64 years were obese [1].
Obesity is a health hazard linked with several
serious medical conditions such as type II diabe-
tes, heart disease, hypertension, and stroke. It has
123
282
also been associated with higher rates of certain
types of cancer, e.g. cancer of the colon, rectum,
or prostate for men, and cancer of the gall
bladder, breast, uterus, cervix, or ovaries for
women [1, 2].
As a rule, patients with end-stage renal disease
(ESRD) on maintenance dialysis have a poorer
outcome, compared to the general population [3–
5]. As numerous reports indicate, low body mass
index (BMI), or weight-for-height [6], as well as
reduced serum total cholesterol or serum creat-
inine concentration [7], are strongly associated
with increased morbidity and mortality. It also
seems that low blood pressure, and not hyperten-
sion, appears to be strongly related to poor
outcome in dialysis patients [8–10]. The same
holds true for homocysteine levels [12], advanced
glycation end products [13] and other traditional
risk factors. These paradoxical observations have
been referred to as ‘‘reverse epidemiology’’ [14,
15] or ‘‘risk factor paradox’’ [16–18].
High BMI has generally been associated with
improved survival among chronic hemodialysis
patients [6, 19, 20–23]. However, studies concern-
ing peritoneal dialysis patients have so far yielded
conflicting results on the relationship of BMI and
survival [24, 25]. Therefore, it is not clear which is
the optimal dialysis modality for obese patients
[26]. The purpose of this study was to evaluate the
Canadian data regarding the impact of BMI on
patients’ survival, taking into consideration their
age, race and gender and the prevalence of
diabetes and hypertension.
Patients and methods
Data presented in this paper were collected and
published by the Canadian Organ Replacement
Registry (CORR) [27]. The Canadian Organ
Replacement Registry collects baseline data on
individuals starting renal replacement therapy in
Canada. This includes demographic information,
primary renal diagnosis, the presence of coronary,
cerebral and peripheral vascular disease, chronic
lung disease, cancer, and any miscellaneous co-
morbid condition which the reporting centre
believes will affect survival. Change of dialysis
modality, kidney transplant, and death are
reported to the register.
123
Int Urol Nephrol (2007) 39:281–288
The current data are from an incident cohort of
ESRD patients (n=4056), older than 18 years,
who initiated Peritoneal Dialysis (PD) between
1994 and 1998, in Canada. These patients were
followed up until the end of 2003, for an average
period of 4.31 ± 2.3 years (range 0.1–8 years).
International standard categorization regarding
BMI was used for the stratification of the patients
according to their BMI, that is the lowest BMI
category was below 18.5 kg/m2, the ‘‘normal’’
ranged between 18.5 kg/m2 and 24.9 kg/m2, the
‘‘overweight’’ patients had BMI 25–29.9 kg/m2
and then the ‘‘obese’’ patients those with a BMI
above 30 kg/m2.
An intent-to-treat Cox regression analysis was
performed, adjusting for age, gender, race, initial
diagnosis, primary disease, and BMI. Patients
were censored at loss to follow up, transplanta-
tion, and the end of the observation period but
not at a switch to hemodialysis.
Kaplan–Meier survival analysis was used to
plot unadjusted survival curves of the patients by
categories of BMI (those with BMI ‡ 30 kg/m2
vs. lower and as quartiles; narrower categories of
BMI were not practical due to sample size
limitations) and sex.
Diabetics were defined on the basis of either
primary diagnosis or reported diabetic co-
morbidity.
Results
There were 4054 patients who initiated PD during
the years 1994–1998 in Canada and for whom there
was a BMI at the initiation of PD, 1742 females
(43%) and 2312 males (57%). Their mean age was
58 ± 15.4 years (range 18–94). There were 3058
(75.4%) Caucasians, 137 (3.4%) Blacks, 120 (3%)
First Nations, and the remaining 739 (18.2%)
belonged to various other races. Diabetes, both
type I and type II, was the primary disease for 1471
(36.2%) of them, chronic glomerulonephritis for
781 (19.3%), hypertension/nephrosclerosis in 749
(18.5%) patients, and various other nephropathies
in 1053 (26%) patients. Their BMI distribution is
shown in Table 1.
In Kaplan–Meyer survival analysis, using
a cut-off value of 30 kg/m2, patients with
Int Urol Nephrol (2007) 39:281–288
Table 1 BMI of the patients
2
BMI (kg/m ) PAT. Number %
<18.5 1130 27.8
19–24.9 1163 28.7
25–29.9 1214 30
>30 547 13.5
BMI > 30 kg/m2 did not have a statistically
significant difference in the overall survival rates
than those with a BMI < 30 kg/m2 (Fig. 1). More
specifically, 3- and 5-year survival was 62.9% and
49.3%, respectively, for the BMI > 30 kg/m2
group and 62.6% and 52% for the BMI < 30 kg/
m2 (P = N.S.). There seemed to be a trend
towards better survival for the BMI > 30 group
during the first three years, but it was reversed
after the fourth (Fig. 1).
Grouped by sex and BMI (again with a cut-off
value of 30 kg/m2), females with BMI > 30 kg/m2
had worse overall survival than males with
BMI > 30 kg/m2, but the difference was not
statistically significant. Conversely, females with
BMI < 30 kg/m2 had better survival than males
with BMI < 30 kg/m2, again not statistically sig-
nificant. Males with BMI < 30 kg/m2 did not have
significantly different survival than those with
BMI > 30 kg/m2 (Fig. 2). On the contrary, fe-
males with BMI < 30 kg/m2 had significantly
better survival (P < 0.05) than those with
BMI > 30 kg/m2, onwards from the second year
(Fig. 2).
In Cox multivariate regression analysis, the
patients’ sex was not a significant factor for
survival. Black race was a protective factor while
advancing age, diabetes, and hypertension as a
BMI<30 BMI>30
Fig. 1 Survival of ESRD Patients who started on Perito-
neal Dialysis between 1994 and 1998 by BMI
283
cause for renal failure, were significant risk
factors for mortality (Table 2).
After dividing the patients into quartiles and
using the BMI 19–25 kg/m2 group as reference,
patients with BMI < 18.5 kg/m2 had a signifi-
cantly higher death hazard ratio (Table 3). On the
other hand, BMI > 30 kg/m2 was not associated
with decreased death hazard ratio, nevertheless
indicating that this group had at least as good
survival as the rest of the patients (Table 3).
Discussion
Several studies over many years have shown that
the association between BMI and survival in
hemodialysis patients differs from that seen in the
general population. Most studies have shown an
inverse relationship, with higher BMI associated
with longer survival.
The first one to report on this phenomenon of
reverse epidemiology was the Diaphane Collab-
orative Study [28] in France. They reported on
the paradoxical observation of a lack of increase
in mortality with high BMI. Subsequently, Leavey
et al. in 1998, confirmed that there is no associ-
ation between higher BMI and increased mortal-
ity risk in a sample of 3607 MHD patients in the
United States Renal Data System (USRDS) [29].
Fleischmann et al. described for the first time a
significantly higher survival rate for MHD
patients with BMI ‡ 27.5 than for those with
BMI = 20–27.5 or BMI: <20 [30]. Wolfe et al.,
studied 9165 MHD patients and found that body
weight, body volume, and BMI, were indepen-
dently and inversely related to mortality [31].
Similarly, Port et al. showed that the lowest BMI
group had a 42% higher mortality risk than did
the highest BMI tertile [32]. Kopple et al evalu-
ated 12965 MHD patients and found that mor-
tality rates decreased as weight-for-height ratio
increased [33]. The Dialysis Outcomes and
Practice Patterns Study (DOPPS) also found an
inverse BMI-mortality relation in MHD subpop-
ulations [34].
Lowrie et al. [35] analyzed survival in 43334
HD patients. The log of risk decreased in roughly
linear fashion for increasing weight, weight for
height, and BSA. Glanton et al. [36] found that
123
284 Int Urol Nephrol (2007) 39:281–288

Fig. 2 Survival of
Patients on PD by Sex
and BMI

obese patients had a higher unadjusted and case-

Table 2 Cox Regression of Factors Associated with mix adjusted 2-year survival after control for all
Mortality among Peritoneal Dialysis Patients, Canada
comorbidities and risk factors; however, the
Death hazard ratio 95% C. I. relation was not uniform and was stronger in
African Americans.
Age 18–34 0.45 0.3–0.7
Age 35–44 Reference Johansen et al. [37] found that even an
Age 45–65 1.88 1.57–2.26 extremely high BMI was associated with in-
Age 65+ 4.6 3.9–5.59 creased survival and reduced risk of hospitaliza-
Glomerulonephritis Reference
tion. This did not hold true for Asian Americans.
Polycystic 0.99 0.81–1.22
Drug-Induced 2.73 1.83–4.06 Other estimates of adiposity and fat mass yielded
Hypertension 2.1 1.7–2.5 similar results.
Diabetes 3 2.5–3. 6 Kalantar-Zadeh et al. [38] recently examined
Other 1.6 1.4–1.9
the effect of both baseline BMI and changes in
Caucasians Reference
First Nations 1.23 0.97–1.57 BMI over time on all-cause and cardiovascular
Black Race 0.57 0.47–0.74 mortality in MHD patients. They found that
Others 0.68 0.6–0.76 obesity was associated with survival advantages.
Males Reference
Moreover, they showed for the first time that
Females 0.98 0.9–1.07
weight loss, while on dialysis, is associated with
increased mortality, whereas weight gain confers
additional survival advantages.
Beddhu et al. [39] suggested that the protective
effect conferred by high BMI is limited to those
Table 3 Cox regression analysis of survival of Peritoneal
Dialysis Patients, by quartiles of BMI patients with normal or high muscle mass.
Very few studies have failed to show survival
BMI Death hazard ratio Confidence interval
advantage of obesity in MHD patients. Thus,
<18.5 1.3 1.1–1.6 Kaizu et al. [40] in 116 non-diabetic Japanese
19–24.9 Reference MHD patients, showed that patients with
25–29.9 0.94 0.86–1.04 BMIs <16.9 and >23.0 had lower survival rates
>30 1.009 0.89–1.14
than did patients with BMIs = 17.0–18.9 kg/m2.

123
Int Urol Nephrol (2007) 39:281–288
Moreover, BMI may interact with race and sex to
predict long-term survival in dialysis patients. In
Kutner and Zang’s study, black females, black
males, and white males with high BMIs had
reduced risk of death, whereas high BMI was not
associated with survival in white females [41].
Research in the field of Peritoneal Dialysis has
in most [42–47], but not all [48–50] cases yielded
similar results of beneficial effects of high BMI on
patient survival. In the CANUSA study, a 1%
increase in lean body mass percentage was asso-
ciated with a 3% decrease in the relative risk of
death [42, 43]. McCusker et al. [44] found a
significantly lower patient survival rate in PD
patients with lower LBM. Johnson et al. [45]
studied the relationship of BMI with survival in a
limited number of PD patients and found that
high BMI conferred a significant survival advan-
tage in the PD population. Chung et al. [46]
described a similar association between ‘‘Fat-free/
edema-free body mass’’ and mortality in Korean
PD patients. Snyder et al. [47] conducted the
largest epidemiologic study in PD, including
46,000 US Medicare patients. They found that
although they had lower transplantation and
technique survival rates, high-BMI PD patients
survived longer than did those with lower BMIs,
for the first two years.
Finally, very recently, Ramkumar et al. [48]
examined the relationship between BMI, muscle
mass and survival in 10,140 incident PD patients.
They concluded that those patients with high
BMI and high or normal muscle mass had the best
survival.
In contrast to the previous reports, several
studies in PD patients found no survival advan-
tage for high BMI, or even reported a higher risk
of death in obese PD patients. Thus, Aslam et al.
[24] compared 2-year survival of 104 PD patients
with a BMI > 27 (high BMI) and 104 PD patients
with a BMI of 20–27 (normal BMI) after match-
ing for age, sex, presence of diabetes, and
Charlson comorbidity index. BMI was not a
predictor of patient mortality or technique sur-
vival when controlled for initial albumin, creati-
nine kinetics, and initial Kt/V.
In a prospective study, conducted by Fried
et al., regarding method and patient survival the
outcome of 343 incident PD patients was not
285
influenced by body weight or body surface area.
The authors concluded that large patients do as
well as smaller patients on PD and that size alone
should not preclude patients from PD [49].
In a survey performed in Australia and New
Zealand over an 11-year period, McDonald et al
examined all new adult patients (n = 9679) who
underwent ‘‘an episode’’ of PD treatment. In a
multivariate analysis, high BMI was indepen-
dently associated with death and technique failure
during PD treatment, except among patients of
Maori/Pacific Islander origin, for whom there was
no significant relation between BMI and mortality
risk during PD treatment. The mortality risk was
lowest for BMI values of 20. They concluded
that high BMI at the start of PD is a significant
risk factor for death and technique failure [50].
Abbott et al. [51] recently performed the
USRDS Dialysis Morbidity and Mortality Wave
II Study among 1675 MHD and 1662 PD patients
and found that 5-year survival was 39.8% for
MHD patients with BMIs ‡ 30 compared with
32.3% for those with lower BMIs (P < 0.01 by
log-rank test). However, 5-year survival above or
below BMI 30 was not significantly different in
PD patients (38.7% for patients with a BMI > 30
and 40.4% for a BMI < 30). Their conclusion was
that any survival advantage associated with obes-
ity among chronic dialysis patients is significantly
less likely for peritoneal dialysis patients, com-
pared to hemodialysis patients.
Stack et al. (52) examined differences between
PD and MHD patients in a cohort of 134,728
incident ESRD patients from the USRDS. In
MHD patients, the adjusted risk of death was
greatest for patients with a BMI < 20.9 and
lowest for patients with a BMI > 30.0 compared
with the reference group (BMI: 23.5–26.1). For
PD patients, the mortality risk was also higher for
patients with a BMI < 20.9, but no survival
advantage was associated with higher BMI values.
They concluded that the selection of HD over PD
was associated with a survival advantage in
patients with a large BMI.
In the Canadian cohort of incident PD
patients, Cox analysis showed that patients with
BMI < 18.5 had an increased death hazard ratio.
These findings are not surprising, since most
studies agree that low BMI is associated with
123
286
poor survival [42–47]. Even McDonald et al. [50],
who proposed that a BMI of ~20 kg/m2 is consis-
tent with the best survival, agree that exception-
ally low BMIs confer increased mortality.
The overall 5-year survival of patients with
BMI > 30 kg/m2 was the same as those with
BMI < 30 kg/m2. Snyder et al. [47] found better
survival in obese PD patients, while Stack et al.
[52], McDonald [50] et al. and Abbott et al. [51]
found worse.
Actuarial analysis, taking into consideration
both the BMI and the sex of the patients, showed
significantly better survival for women with
BMI < 30 kg/m2 compared with those with
BMI > 30 kg/m2 (P < 0.05). Such a difference
was not observed between men with BMI above
and below 30 kg/m2. Multivariate Cox regression
analysis, after corrections for age, race, primary
disease, and BMI showed that the patients’ sex
was not a significant survival factor. Most other
authors have not found a connection either,
except Kutner and Zang who found that high
BMI did not exert a protective role on Caucasian
women [41].
Black race was a protective factor, and this is in
agreement with all other authors. Advancing age,
diabetes, hypertension, and drug-induced
nephropathy were factors that affected negatively
the survival of the patients in a statistically
significant way.
An observational study of this kind is not
optimal for making causal inferences. Neverthe-
less, we think that PD patients with high BMI fare
at least as well as any other, with the possible
exception of female patients. Perhaps, maintain-
ing a higher-than-average BMI to preserve
‘‘nutritional reserve’’ may help to reduce the
mortality and morbidity rates associated with PD.
The fact that we did not find a statistical signif-
icance regarding survival and BMI (although the
confidence interval barely exceeded 1, falling just
short of statistical significance), was perhaps due
to our using the patients’ BMI at initiation of PD,
and not re-evaluating it during the treatment
period, which is a weakness not only of our study,
but of most similar ones. On the other hand, our
patients’ sample covers all of Canada, and our
follow-up time is among the longest in the
literature, facts that give strength to our study.
123
Int Urol Nephrol (2007) 39:281–288
Table 4 Possible mechanisms for reverse epidemiology
of obesity in ESRD patients
Malnutrition-inflammation complex syndrome (cachexia
in slow motion)
Time discrepancies among competitive risk factors:
overnutrition compared with undernutrition
More stable hemodynamic status in obese patients
Tumor necrosis factor-a receptors in obesity
Neurohormonal alterations in obesity
Endotoxin-lipoprotein hypothesis
Reverse causation
Survival bias
Alteration of conventional risk factors in uremic milieu
Predominance of reverse epidemiology in the history of
mankind
The whole idea of reverse epidemiology may
appear confusing, because high BMI is an estab-
lished risk factor for CVD and poor outcome in
the general population. In two excellent review
articles, Kalantar-Zadeh et al. [53] and Kopple
[54] deal extensively with the possible causes of
reverse epidemiology. The most probable ones
are summarized in Table 4.
In conclusion, patients with high BMI fare as
well as patients with normal BMI on Peritoneal
Dialysis. Black race is a protective factor, while
diabetes and hypertension as cause for renal
failure are associated with enhanced death hazard
ratio. Patients with high BMI should therefore
not be discouraged from initiating PD purely on
the basis of size.
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