You are on page 1of 6

CE: Tripti; MNH/290206; Total nos of Pages: 6;

MNH 290206

REVIEW

CURRENT
OPINION Nephrolithiasis in women: how different from men?
Lada Beara-Lasic and David S. Goldfarb

Purpose of review
Men have more kidney stones compared with women; however, the difference is progressively decreasing.
The reasons for higher prevalence of stones in men, as well as increasing prevalence in women, is a
subject of ongoing speculation. In this review, we summarize the evidence of differences between men and
women and expand on the speculative causes.
Recent findings
Stone incidence is rising in women and adolescent girls. Stone disease is more heritable among men than
women, and women demonstrate greater influence of the unique environment. Women under the age of
50 years who have been pregnant, have more than double the odds of kidney stones compared with those
who have never been pregnant. Women are more burdened with obesity, bariatric surgery and dieting, all
associated with increased stones. Women have higher urinary pH because of greater absorption of dietary
organic anions leading to increased urinary citrate, compared with men, and they differ in tubular calcium
handling.
Summary
It is obvious that the cause of stones in men and women is complex and requires further study. Potential
clues offered are in the change of the female environment, influencing increasing incidence in stones,
particularly of younger women and female adolescents.
Keywords
calcium, calculi, men/boys, nephrolithiasis, renal, urolithiasis, women/girls

INTRODUCTION women in all age groups, but the difference between


Kidney stones affect a significant number of patients men and women was lowest in the ages 10–29 years
(approximately 1/11 in the United States) with and more than 90 years [7]. Additionally, the analy-
increasing incidence in the United States and the sis of the population data from the National Health
rest of the world [1,2]. Men are still more commonly and Nutrition Examination Survey data (NHANES)
affected, with a ratio currently less than 2 : 1 and between 1976 and 1994 demonstrated that 20–29-
progressively decreasing. Recent local population- year-old women had an approximately 50% higher
based data indicate stone incidence is rising in the prevalence of stones than men of the same age [8].
previously lower risk groups of women and adoles- More recently NHANES data from the 2007–2012
cent girls [3–5]. In the Olmstead County adult pop- for adults younger than 50 years, showed no differ-
ulation data from 1984 to 2012, it was observed that ence in stone prevalence between men and women,
women ages 18 to 39 years had the highest absolute and this finding continued to be present in the
&&

increase in the incidence of confirmed symptomatic subpopulations of age by decade [9 ]. Unfortu-


kidney stones [4]. nately, cross-sectional survey data of NHANES do
Interestingly, the analysis of the 43 545 individ-
uals’ first stones submitted to the Mayo Clinic Metal
Laboratory during year 2010, the number of stones Nephrology Division, NYU Langone Health, NYU School of Medicine,
and New York Harbor VA Healthcare System, New York, New York, USA
submitted was even greater among adolescent girls
(10–19 years old) and young adult women (20–29 Correspondence to Lada Beara-Lasic, MD, MS, Nephrology Section,
New York Harbor VA Healthcare System, Clinical Assistant Professor of
years old), when compared with men of the same Medicine, New York University School of Medicine, New York Harbor
age. It was almost the same for men and women VAMC, 423 E. 23 Street, New York, NY 10010, USA.
greater than 90 years. In the ages between 10 and Tel: +1 212 686 7500 3880; fax: +1 212 951 6842;
29 years, women submitted about 60% of all stones e-mail: lada.bearalasic@nyulangone.org
[6]. Similarly, in a French study based on analysis of Curr Opin Nephrol Hypertens 2019, 28:000–000
27 980 calculi, men submitted more stones than DOI:10.1097/MNH.0000000000000577

1062-4821 Copyright ß 2019 Wolters Kluwer Health, Inc. All rights reserved. www.co-nephrolhypertens.com

Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CE: Tripti; MNH/290206; Total nos of Pages: 6;
MNH 290206

Clinical nephrology

the higher urinary pH. (Higher urine pH titrates a


KEY POINTS proton off monobasic H2PO4 and converts it into
 Men have more kidney stones than women; ratio is less the divalent dibasic HPO4¼, which readily precip-
than 2 : 1 and progressively decreasing and women itates with calcium, a divalent cation.) Large epide-
ages 18–39 years have the highest absolute increase miologic studies have shown that the pH of 24-h
in the incidence of confirmed symptomatic urines in women on a free-choice diet, are higher
kidney stones. than in men [11–13]. This finding of higher urinary
 Women have higher urinary pH because of greater pH in women largely explains higher prevalence of
absorption of food organic anions leading to increased CaP stones in women compared with men, although
urinary citrate, compared with men. calcium oxalate stones (CaOx) are still the most
prevalent stones in both sexes [10]. The sex pH
 Women have more calcium phosphate and
difference has been attributed to differences in diet;
struvite stones.
however, the recently published work by Worcester
 Stone disease is more heritable among men than et al. who studied seven normal men and seven
among women, and women demonstrate greater women on a standardized diet, demonstrated that
influence of the unique environment. women have higher urinary pH only in fed and not
 Women under the age of 50 years who have been in fasting state, as a result of greater absorption of
pregnant, have more than double the odds of kidney food anions. Urine citrate was higher in women
stones compared with those who have never been than men in the fed state, and fractional excretion
pregnant and the prevalence and odds of stones &&
of citrate was higher in women than men [14 ]. The
increase with increasing number of pregnancies. basis for these findings is currently not clear.
According to the recent analysis of the first stones
submitted by patients to the Mayo Clinic Metal Lab-
not capture types of stones; therefore, they do not oratory during year 2010, hydroxyapatite stones
provide insight on the cause of recent increasing (associated with higher urinary pH) were indeed
incidence of stones in women. more common among young women, the demo-
The most common types of stones are calcium graphic group who had the highest increase in the
oxalate (CaOx), and about 80% of all stones are incidence rate of kidney stones [6]. In fact, in women
CaOx and/or calcium phosphate (CaP). Most CaP between the ages of 20 and 29 years, the percentage of
stones are composed of hydroxyapatite. The data on hydroxyapatite stones was even greater than the
stone distribution by type submitted from multiple percentage of CaOx stones (the only period where
referral laboratories are similar. From the Mayo CaOx was not the most common stone type). The
Clinic 2010 first stone analysis, 67% of stones were question remains, what is the reason for this increase?
CaOx, followed by hydroxyapatite (16%), uric acid If the rise in pH in women is noticed only in fed states,
(8%), struvite (3%), brushite (0.9%), and cystine can we speculate that a change in diet in women is
(0.35%) [6]. The proportion of hydroxyapatite and driving this change? What else has changed in the
struvite stones is higher in women compared with environment of adolescent and young women to lead
men; in fact, women submitted the majority of them to form more CaP stones?
hydroxyapatite stones (65%) and struvite stones
(65%). Women made the highest percentage of
hydroxyapatite between ages 20 and 39 years and DIFFERENCE OF KIDNEY CALCIUM
struvite stones after age 70 years. The uric acid stone HANDLING BETWEEN MEN AND WOMEN
proportion increased significantly after the age of WITH HIGHER URINARY CALCIURIA
50 years for both sexes. In another study of 1201 The cause of higher urinary calcium excretion
stone formers, men and women, followed over three among calcium stone formers with higher urine
decades, the percentage of CaP in both sexes calcium excretion is reduced renal tubular calcium
increased about three-fold and the stones from reabsorption, detected using the endogenous lith-
women had higher percentage CaP composition. ium clearance measurements, in the fasting state but
This study also confirmed younger onset of stone most pronounced after eating [15]. Using the same
disease in CaP stone patients for both sexes [10]. model, the primary mechanism detected in women
with higher urinary calciuria was decreased distal
nephron calcium reabsorption compared with nor-
DIFFERENCE OF URINE PH BETWEEN MEN mal women, whereas in men, it was decreased prox-
AND WOMEN imal tubular calcium reabsorption, with a more
Urinary pH is normally maintained close to 6, which modest reduction in distal calcium reabsorption
avoids precipitation of uric acid at lower, and CaP at when compared with normal men [16].

2 www.co-nephrolhypertens.com Volume 28  Number 00  Month 2019

Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CE: Tripti; MNH/290206; Total nos of Pages: 6;
MNH 290206

Nephrolithiasis in women Beara-Lasic and Goldfarb

IMPACT OF PREGNANCY AND WOMEN AND HORMONAL THERAPY


LACTATION ON KIDNEY STONES Oral contraception has been used as a significant
mode of contraception: the nationally representa-
During pregnancy, women’s calcium and phospho- tive survey conducted in 2004 showed 38% of all
rus metabolism changes to adapt to the skeletal women using oral contraceptive methods [20]. Ado-
needs of the fetus. Increased intakes are not required lescence is a critical period for bone development as
in women who consume adequate calcium and the peak bone mass occurs by the end of the second,
there are not thought to be long-term consequences or early in the third decade of life [21]. Oral contra-
for the maternal skeleton, except for women with ceptives taken in adolescence decrease the peak
low mineral intake or preexisting disorders, because bone mass and are associated with the decreased
of the doubling of the efficiency of intestinal cal- bone turnover markers, increasing the risk of osteo-
cium absorption during pregnancy. This effect is &
porosis [22 ,23]. Could we speculate that the
mediated by the increase in the parathyroid hor- increasing use of oral contraceptives may have influ-
mone-related protein (PTHrP) and also estradiol, enced rising incidence of stones in the adolescent
prolactin, and placental lactogen causing the stimu- girls? This area requires further study.
lation of CYP27b1 to produce increased levels of 1,25-
dihydroxy vitamin D (1,25-D) and suppression of
parathyroid hormone (PTH). Levels of 25-hydroxy BONE DISEASE AND KIDNEY STONES IN
vitamin D do not appear to have a significant role in MEN AND WOMEN
pregnancy, as supplementation with as much as 5000 Low bone mineral density (BMD) has been associ-
units daily did not alter maternal serum Ca, P, PTH or ated with kidney stones in smaller studies as well as
blunt the rise in 1,25 D. The hormonal changes result population-based studies [24–26]. However, these
in the increase of 24 h urinary calcium, likely a con- studies did not differentiate between men and
sequence of increased intestinal absorption and the women or analyzed men only. In the cross-sectional
increased filtered load of calcium with the increased analysis of NHANES III data, a history of any kidney
glomerular filtration rate of pregnancy [17]. In addi- stones (not limited to calcium stones) was signifi-
tion to higher calciuria, urines of pregnant women cantly associated with lower BMD in men but not in
have greater uricosuria, oxaluria and elevated urine women [27]. An earlier population-based study
pH, which increases calcium phosphate urinary demonstrated the risk of vertebral fracture to be
supersaturation [18]. greatly increased among men who formed kidney
During lactation, intestinal calcium and phos- stones, and only to be mildly elevated among
phorus absorption falls to nonpregnant values, coin- women [28]. Looking at the female data only, the
ciding with the fall of 1,25-D, despite persistently prospective analysis of 96 092 women in the Nurses’
high PTHrP. The calcium needed for breast milk is Health Study II, showed increased adjusted relative
now released from the bone. At the same time, the risk for an incident kidney stone for participants
tubular maximum for calcium increases and the with history of low bone density compared with
fractional excretion of calcium decreases, likely participants without [29]. In a study of postmeno-
mediated by PTHrP. Any additional calcium taken pausal women with osteoporosis, higher urinary
from supplements or from food will increase urinary calcium excretion was present in 19% and was
calcium without affecting milk calcium or amount found to be the most important predictor of low
of bone resorbed. This information is important for bone mass [30]. This implicates more complex
our hypercalciuric women during lactation. A mod- mechanisms, such as potential use of hormones in
est increase in intestinal calcium absorption might female bone loss and points to the differences
occur during postweaning recovery; female bone is between men and women.
thought to completely recover its mineral content
3–6 months after ending lactation [17].
The data have not consistently shown increase of OBESITY/WEIGHT REDUCTION
kidney stone incidence during pregnancy; however, SURGERIES/EATING DISORDERS AND
the potentially lithogenic state of pregnancy may KIDNEY STONES IN MEN AND WOMEN
carry a risk of future stone development. NHANES Women have been highly affected in the obesity
data analysis from 2007 to 2012 demonstrated that epidemic. According to the 2013–2014 NHANES
the odds of nephrolithiasis are more than two-fold in data, the age-adjusted prevalence of obesity was
women who have been pregnant compared with 35% for men and 40.4% for women [31]. Obesity
those who have never been pregnant [19]. The prev- is associated with lower urinary pH increasing prob-
alence and odds of nephrolithiasis increased with the ability of uric acid crystallization as well as increased
increasing number of pregnancies. intake of salt that increases urinary calcium

1062-4821 Copyright ß 2019 Wolters Kluwer Health, Inc. All rights reserved. www.co-nephrolhypertens.com 3

Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CE: Tripti; MNH/290206; Total nos of Pages: 6;
MNH 290206

Clinical nephrology

excretion. Insulin resistance, associated with the and laxative abuse; however, there is a paucity of
obesity epidemic, may also possibly increase intes- cases reported. Possible links with kidney stones are
tinal absorption and urinary excretion of calcium extracellular fluid volume depletion and electrolyte
[32]. From the 11 099 stones submitted to a Labora- and acid–base disturbances, including hypokalemia
tory for Stone Research in Massachusetts in the leading to hypocitraturia, both favoring the forma-
period from 1990 to 2010, there was a significant tion of kidney stones. In addition, ammonium acid
increase in the proportion of uric acid stones only in urate stones, more commonly seen in underdevel-
women; it was not seen in men [33]. However, men oped countries, were reported in women with laxa-
were still more likely to submit uric acid stones (10.3 tive abuse and bulimia [43]. It is of interest to note
versus 5.5%), compared with women and there was a that women with anorexia and bulimia have associ-
significant increase of uric acid stones in both sexes ated loss of bone mineral density, which is even
after approximately age 50 years, uric acid constitut- noted in women with normal weight bulimia, indi-
ing more than 20% of stones in those greater than cating causes other than weight loss affecting bone
90 years old. In general, the sex differences in stone mineral metabolism.
composition were much less prominent over age
70 years and most marked under age 30 years, con-
sistent with the previously discussed data. Stone INFECTIONS/ANTIBIOTICS AND STONES
analysis from a Korean study has also shown obesity IN MEN AND WOMEN
associated with higher likelihood of uric acid and Female children and adult women have higher prev-
CaOx stones compared with the occurrence of mixed alence of urinary tract infections, and as expected,
CaOx/CaP stones, and CaP stones [34]. data indicate that women with calcium kidney
The number of bariatric surgeries is increasing stones have more urinary infections [44]. Women
worldwide and 70–80% of patients undergoing sur- also have more struvite stones, occurring because of
gery are women [35,36]. Patients with weight reduc- recurrent urinary tract infections with urease-pro-
tion surgery, specifically intestinal bypass (Roux-en- ducing organisms, such as Proteus spp. [6].
Y), will have increased CaOx stone formation. In Use of antibiotics has also been associated with
these patients, fat malabsorption causes increased kidney stones, supporting the hypothesis that
calcium binding in the intestinal lumen, and con- changes in the intestinal microbiome induced by
sequently increased free oxalate absorption, leading antibiotics modulates the intestinal handling of
to the increase of urinary oxalate excretion. Bile salts calcium and oxalate to favor stone formation. In a
also increase colonic permeability and facilitate oxa- large case–control study from United Kingdom, the
late absorption. Gastric banding, which does not exposure to five different antibiotic classes given for
lead to steatorrhea, does not increase urinary oxalate varying indications was associated with increased
excretion [37–39]. odds of nephrolithiasis, particularly in younger
On the other side of the spectrum, dieting has ages. Both cohorts included 35% women; however,
been associated with lower bone mineral accrual men and women were not compared [45]. In the
and more severe eating disorders with kidney more recent analysis of The Nurses’ Health Study
stones. Girls are more affected. According to the (NHS) I and II cohort, the use of antibiotics for a total
recent nationally representative data from US high of 2 months or more during early-to-middle adult-
school students surveyed from 2010 to 2011, 61% of hood was independently associated with higher
girls and 32% of boys reported trying to lose weight; subsequent risk for developing kidney stones in later
17% of girls and 7% of boys reported fasting for more life [46]. Kidney stone formers are indeed found to
than 24 h and 6% of girls and 2.5% of boys reported have different intestinal microbiome composition
vomiting or laxative use within 30 days of survey [47,48]. However, no comparison between men and
[40]. Girls who first reported dieting to lose weight women is available.
by age 11 years showed a significantly lower bone
mineral accrual compared with girls who first
reported dieting after 11 years or not at all [41 ].
&
CONCLUSION
Dietary restraint has been associated with lower The reasons for overall increased prevalence of
levels of bone formation markers in young adult stones in men compared with women remains a
women [42]. Is the dietary restriction and related topic of ongoing speculation. One of the factors
behaviors influencing stone formation in the cohort commonly hypothesized is the difference in diet
of young adolescent girls with increasing incidence influencing solute excretion and urine volume.
of stones? This area has not been investigated. The NHANES 2007–2012 for adults younger than
Kidney stones are noted to be associated with 50 study has analyzed the three most common
eating disorders, such as anorexia nervosa, bulimia, dietary factors associated with stone formation

4 www.co-nephrolhypertens.com Volume 28  Number 00  Month 2019

Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CE: Tripti; MNH/290206; Total nos of Pages: 6;
MNH 290206

Nephrolithiasis in women Beara-Lasic and Goldfarb

2. Sorokin I, Mamoulakis C, Miyazawa K, et al. Epidemiology of stone disease


and has found that men, as previously hypothe- across the world. World J Urol 2017; 35:1301–1320.
sized, showed higher salt and protein intake. Men, 3. Tasian GE, Ross ME, Song L, et al. Annual incidence of nephrolithiasis among
children and adults in South Carolina from 1997 to 2012. Clin J Am Soc
surprisingly, had a slightly higher water intake than Nephrol 2016; 11:488–496.
&&
women (less than 100 ml) [9 ]. Men are more likely 4. Kittanamongkolchai W, Vaughan LE, Enders FT, et al. The changing incidence
and presentation of urinary stones over 3 decades. Mayo Clin Proc 2018;
to be employed as drivers, or having prostate 93:291–299.
enlargement limiting intake of fluid; however, we 5. Dwyer ME, Krambeck AE, Bergstralh EJ, et al. Temporal trends in incidence of
kidney stones among children: a 25-year population based study. J Urol 2012;
can also speculate that women in their child-rearing 188:247–252.
ages tend to significantly reduce fluid intake and 6. Lieske JC, Rule AD, Krambeck AE, et al. Stone composition as a function of
age and sex. Clin J Am Soc Nephrol 2014; 9:2141–2146.
both sexes tend to drink less fluid in older ages. It is, 7. Daudon M, Doré JC, Jungers P, Lacour B. Changes in stone composition
therefore, not surprising that in the NHANES study, according to age and gender of patients: a multivariate epidemiological
approach. Urol Res 2004; 32:241–247.
urine volume was not found to be significantly 8. Stamatelou KK, Francis ME, Jones CA, et al. Time trends in reported pre-
different. Perhaps the most striking difference valence of kidney stones in the United States: 1976-1994. Kidney Int 2003;
63:1817–1823.
between women and men, in part accounting for 9. Tundo G, Khaleel S, Pais VM. Gender equivalence in the prevalence of
differences in stone prevalence, is that men have && nephrolithiasis among adults younger than 50 years in the United States. J
Urol 2018; 200:1273–1277.
higher urinary oxalate excretion. Study of NHANES data from the 2007–2012 for adults younger than 50 years,
It is evident, however, that the cause of stones is showed no difference in stone prevalence between men and women, present also
in the subpopulations of age by decade.
far more complex. Further subdivisions by the age of 10. Parks JH, Worcester EM, Coe FL, et al. Clinical implications of abundant
patients, might give us clues for better understand- calcium phosphate in routinely analyzed kidney stones. Kidney Int 2004;
66:777–785.
ing. Differences in genetics of men and women 11. Curhan GC, Taylor EN. 24-h uric acid excretion and the risk of kidney stones.
influencing final urine composition, as well as diet- Kidney Int 2008; 73:489–496.
12. Lieske JC, Turner ST, Edeh SN, et al. Heritability of dietary traits that
ing and life events, such as pregnancy and lactation, contribute to nephrolithiasis in a cohort of adult sibships. J Nephrol 2016;
might play a role more significant than previously 29:45–51.
13. Taylor EN, Stampfer MJ, Mount DB, Curhan GC. DASH-style diet and 24-h
suspected. According to our recent study of the 7053 urine composition. Clin J Am Soc Nephrol 2010; 5:2315–2322.
same-sex pairs with kidney stone data from the 14. Worcester EM, Bergsland KJ, Gillen DL, Coe FL. Mechanism for higher urine
pH in normal women compared with men. Am J Physiol Renal Physiol 2018;
Washington State Twin Registry, stone disease was &&

314:F623–F629.
more heritable among men than among women (57 Study comparing seven normal men and seven women on a standardized diet
found that women have higher urinary pH only in fed and not in fasting state, as a
vs. 46%, P < 0.05) and women demonstrated greater result of greater absorption of food anions.
&
influence of the unique environment [49 ]. The 15. Worcester EM, Coe FL, Evan AP, et al. Evidence for increased postprandial
distal nephron calcium delivery in hypercalciuric stone-forming patients. Am J
intriguing question is what is the recent change of Physiol Renal Physiol 2008; 295:F1286–F1294.
the female environment that is influencing increas- 16. Ko B, Bergsland K, Gillen DL, et al. Sex differences in proximal and distal
nephron function contribute to the mechanism of idiopathic hypercalcuria in
ing incidence in stones, particularly of younger calcium stone formers. Am J Physiol Regul Integr Comp Physiol 2015;
women and female adolescents? If we look at our 309:R85–R92.
17. Kovacs CS. Maternal mineral and bone metabolism during pregnancy, lacta-
own individual stone clinic practices, we can cer- tion, and post-weaning recovery. Physiol Rev 2016; 96:449–547.
tainly recognize the multitudes of factors influenc- 18. Smith CL, Kristensen C, Davis M, Abraham PA. An evaluation of the physi-
cochemical risk for renal stone disease during pregnancy. Clin Nephrol 2001;
ing stone formation, and it would be worthwhile 55:205–211.
investigating closer and further to improve both 19. Reinstatler L, Khaleel S, Pais VM. Association of pregnancy with stone
formation among women in the United States: a NHANES analysis 2007
prevention and treatment. to 2012. J Urol 2017; 198:389–393.
20. Frost JJ, Darroch JE. Factors associated with contraceptive choice and
Acknowledgements inconsistent method use, United States, 2004. Perspect Sex Reprod Health
2008; 40:94–104.
None. 21. Baxter-Jones AD, Faulkner RA, Forwood MR, et al. Bone mineral accrual from
8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res
2011; 26:1729–1739.
Financial support and sponsorship 22. Rizzo ADCB, Goldberg TBL, Biason TP, et al. One-year adolescent bone
& mineral density and bone formation marker changes through the use or lack of
None. use of combined hormonal contraceptives. J Pediatr (Rio J) 2018;
95:567–574.
Oral contraceptives taken in adolescence decrease the peak bone mass.
Conflicts of interest 23. Callegari ET, Gorelik A, Garland SM, et al. Bone turnover marker reference
L.B.-L.: none; D.S.G.: consultant: Allena, AstraZeneca, intervals in young females. Ann Clin Biochem 2017; 54:438–447.
24. Keller JJ, Lin CC, Kang JH, Lin HC. Association between osteoporosis and
Retrophin; Equity holder: Dr Arnies. urinary calculus: evidence from a population-based study. Osteoporos Int
2013; 24:651–657.
25. Jaeger P, Lippuner K, Casez JP, et al. Low bone mass in idiopathic renal stone
REFERENCES AND RECOMMENDED formers: magnitude and significance. J Bone Miner Res 1994; 9:1525–1532.
26. Pietschmann F, Breslau NA, Pak CY. Reduced vertebral bone density in
READING hypercalciuric nephrolithiasis. J Bone Miner Res 1992; 7:1383–1388.
Papers of particular interest, published within the annual period of review, have 27. Lauderdale DS, Thisted RA, Wen M, Favus MJ. Bone mineral density and
been highlighted as: fracture among prevalent kidney stone cases in the Third National Health and
& of special interest Nutrition Examination Survey. J Bone MinerRes 2001; 16:1893–1898.
&& of outstanding interest
28. Melton LJ, Crowson CS, Khosla S, et al. Fracture risk among patients with
urolithiasis: a population-based cohort study. Kidney Int 1998; 53:459–464.
1. Scales CD, Smith AC, Hanley JM, Saigal CS; Urologic Diseases in America 29. Prochaska M, Taylor E, Vaidya A, Curhan G. Low bone density and bispho-
Project. Prevalence of kidney stones in the United States. Eur Urol 2012; sphonate use and the risk of kidney stones. Clin J Am Soc Nephrol 2017;
62:160–165. 12:1284–1290.

1062-4821 Copyright ß 2019 Wolters Kluwer Health, Inc. All rights reserved. www.co-nephrolhypertens.com 5

Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
CE: Tripti; MNH/290206; Total nos of Pages: 6;
MNH 290206

Clinical nephrology

30. Giannini S, Nobile M, Dalle Carbonare L, et al. Hypercalciuria is a common Girls who first reported dieting to lose weight by age 11 years showed a
and important finding in postmenopausal women with osteoporosis. Eur J significantly lower bone mineral accrual compared with girls who first reported
Endocrinol 2003; 149:209–213. dieting after 11 years or not at all.
31. Flegal KM, Kruszon-Moran D, Carroll MD, et al. Trends in obesity among 42. Cano Sokoloff N, Eguiguren ML, Wargo K, et al. Bone parameters in relation
adults in the United States, 2005 to 2014. JAMA 2016; 315:2284–2291. to attitudes and feelings associated with disordered eating in oligo-amenor-
32. R€umenapf G, Schmidtler J, Schwille PO. Intestinal calcium absorption during rheic athletes, eumenorrheic athletes, and nonathletes. Int J Eat Disord 2015;
hyperinsulinemic euglycemic glucose clamp in healthy humans. Calcif Tissue 48:522–526.
Int 1990; 46:73–79. 43. Leaf DE, Bukberg PR, Goldfarb DS. Laxative abuse, eating disorders, and
33. Moses R, Pais VM, Ursiny M, et al. Changes in stone composition over two kidney stones: a case report and review of the literature. Am J Kidney Dis
decades: evaluation of over 10,000 stone analyses. Urolithiasis 2015; 2012; 60:295–298.
43:135–139. 44. Parks JH, Coe FL, Strauss AL. Calcium nephrolithiasis and medullary sponge
34. Jeong JY, Doo SW, Yang WJ, et al. Differences in urinary stone composition kidney in women. N Engl J Med 1982; 306:1088–1091.
according to body habitus. Korean J Urol 2011; 52:622–625. 45. Tasian GE, Jemielita T, Goldfarb DS, et al. Oral antibiotic exposure and kidney
35. Gagnon C, Schafer AL. Bone health after bariatric surgery. JBMR Plus 2018; stone disease. J Am Soc Nephrol 2018; 29:1731–1740.
2:121–133. 46. Ferraro PM, Curhan GC, Gambaro G, Taylor EN. Antibiotic use and risk of
36. Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery and endoluminal incident kidney stones in female nurses. Am J Kidney Dis 2019. [Epub ahead
procedures: IFSO Worldwide Survey 2014. Obes Surg 2017; 27:2279–2289. of print]
37. Asplin JR, Coe FL. Hyperoxaluria in kidney stone formers treated with modern 47. Ticinesi A, Milani C, Guerra A, et al. Understanding the gut-kidney axis in
bariatric surgery. J Urol 2007; 177:565–569. nephrolithiasis: an analysis of the gut microbiota composition and functionality
38. Lieske JC, Mehta RA, Milliner DS, et al. Kidney stones are common after of stone formers. Gut 2018; 67:2097–2106.
bariatric surgery. Kidney Int 2015; 87:839–845. 48. Tang R, Jiang Y, Tan A, et al. 16S rRNA gene sequencing reveals altered
39. Liu M, Nazzal L. Enteric hyperoxaluria: role of microbiota and antibiotics. Curr composition of gut microbiota in individuals with kidney stones. Urolithiasis
Opin Nephrol Hypertens 2019; 28:352–359. 2018; 46:503–514.
40. Eaton DK, Kann L, Kinchen S, et al. Youth risk behavior surveillance - United 49. Goldfarb DS, Avery AR, Beara-Lasic L, et al. A twin study of genetic influences
States, 2011. MMWR Surveill Summ 2012; 61:1–162. & on nephrolithiasis in women and men. Kidney Int Rep 2019; 4:535–540.
41. Hohman EE, Balantekin KN, Birch LL, Savage JS. Dieting is associated with Study of the same-sex pairs with kidney stone data from the Washington State
& reduced bone mineral accrual in a longitudinal cohort of girls. BMC Public Twin Registry showed stone disease was more heritable among men than women
Health 2018; 18:1285. and women show greater influence of the unique environment.

6 www.co-nephrolhypertens.com Volume 28  Number 00  Month 2019

Copyright © 2019 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.

You might also like