Introduction

Urolithiasis is a common disease affecting 5–10% of the global population. It has a high recurrence rate of up to 50% at 10 years1. In recent years, a global rise in the prevalence of urinary stone disease among women and men, and further increases are expected due to changes in lifestyle, dietary habits, and global warming2. Urinary stone formation is caused by metabolic disease, genetic factors, and anatomical and functional abnormalities. Conditions such as obesity, type 2 diabetes (T2DM), hypertension (HTN), and metabolic syndrome are risk factors for this pathology3.

Many studies support the crucial role of diet in the formation and prevention of urolithiasis. Nutrition is a key modifiable risk factor associated with urinary stone disease2.

Reduced fluid intake is a major predisposing factor, as low fluid intake is related to less urine production and can predispose to solute hypersaturation and stone formation. Conversely, increased consumption of sugar-sweetened beverages is associated with a higher risk of lithogenesis due to elevated urinary excretion of oxalates, uric acid, and calcium. Calcium, magnesium, or potassium intake may reduce lithogenesis. Similarly, the high consumption of animal proteins, sodium, or sugar can cause stones3,4,5,6.

The association between BMI and urolithiasis is reported with a prevalence of obesity among patients with kidney stone disease ranging from 10 to 35%. The correlation between obesity and kidney stones is demonstrated by epidemiological study, with urolithiasis higher in obese (11.2%) and overweight (9.1%) patients7.

Obesity is associated with increased excretion of solutes (mainly calcium, oxalates, and sodium) and a lower urinary pH, all factors contributing to stone formation. Calcium oxalate and uric acid stones are common types of stones diagnosed in obese patients, and improper diet plays a major role in their pathophysiology7,8.

Bariatric surgery (BS) is highly effective for the prolonged treatment of morbid obesity, leading to substantial weight loss, reducing mortality, and a lower incidence of obesity-related comorbidities, including diabetes, HNT, cardiovascular disease, and obstructive sleep apnea. Surgical treatment may lead to long-term complications such as nutritional deficiencies, biliary lithiasis, abnormal bone and mineral metabolism, and nephrolithiasis9,10.

This risk of developing urolithiasis in bariatric patients increases by 7.6% for 5 years post-surgery and higher after malabsorptive procedures. Stones typically develop around 1.5 years post-surgery. Hypo- and malabsorptive procedures predispose to fat malabsorption, enhancing free oxalate absorption by sequestration of calcium in fat. Hyperoxaluria is the most common disorder in patients receiving BS. The underlying mechanism is not understood but is linked to nutrition imbalances, fat malabsorption, and alteration of the intestinal microbiota11,12,13.

The study aimed to evaluate the incidence of urolithiasis for 2 years in patients who underwent BS in an Italian center of excellence, focusing on the impact of different procedures and the role of nutritional counseling as a reducing risk factor.

Methods

The study was prospectively conducted by two Academic Center (General Surgery and Urology Division) part of the same Institution between January 2020 and September 2022. All methods were carried out in accordance with relevant guidelines and regulations. All experimental protocols were approved by the Department of Medico-Surgical Sciences and Biotechnologies with protocol n 0001612 of December 16, 2019. Informed consent was obtained from all subjects.

Patients attending consecutive follow-up visits up to the second year following primary BS were included.

Nutritional counseling

Was performed, and anthropometric parameters (weight, height, BMI, and %EWL) were measured pre- and post-surgery. After overnight fasting, patients were weighed barefoot and in light clothing to the nearest 0.1 kg. Height was measured using a fixed wall stadiometer; height and weight were recorded, and BMI (kg/m2) was calculated. Fluid intake and supplementation were assessed during follow-up visits.

All patients followed our post-operative nutritional protocol: liquid (up to 1 week), pureed (2 or 3 weeks), soft solid (progress as tolerated), and firmer, regular food.

After the first post-operative month, patients were advised to meet minimal carbohydrates (130 g/day) and fat (20 g/day) needs. The dietitian aimed to advise a balanced diet, including adequate servings from all food groups, with protein of 1.1 g/kg ideal body weight, and to limit or exclude added sugar, concentrated sweets, fruit juice, fried foods, carbonated drinks, caffeine, and alcohol. Daily intake of a minimum of 1.5 L of water was recommended.

Urological counseling

Pre-operative urinary stone disease was excluded by evaluating the upper urinary tract through an abdominal ultrasound performed one month before surgery and urine analysis. Patients with a history of urinary stone disease, caliectasis, hydroureteronephrosis, and/or kidney stones discovered at the pre-operative ultrasound evaluation were excluded from the study. Patients with urine analysis positive for urinary crystals were also excluded from the study.

Follow-up period

BS patients attended ambulatory visits every 1st, 3rd, 6th, and 12 months for the first year and then every six months, receiving surgical/nutritional and psychological assessment. At 2 years follow-up, all the patients underwent urine analysis. All patients positive for urinary crystals were referred to the Division of Urology to evaluate the possible presence of urinary stones. According to the European Association of Urology (EAU) guidelines, patients receive a complete urological evaluation. Urolithiasis (in case of urine analysis positivity) was evaluated by an abdominal computed tomography (CT) without contrast (Fig. 1).

Fig. 1
figure 1

Flowchart of the study.

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Statistical methods

Continuous variables assuming normal distribution are expressed as mean ± standard deviation (SD), while categorical variables are presented as numbers (n) and proportions (%). Kidney stone formation risk was evaluated using Cox regression, presenting hazard ratios (HRs) and 95% confidence intervals (CIs) as measures of association. Preoperative variables were assessed as risk factors for postoperative kidney stones among the operative group using unadjusted Cox regression and further in a multivariable model including all preoperative variables. A second Cox regression model, including postoperative weight reduction at 2 years after surgery, was performed and adjusted for all preoperative variables. Med Calc (version 22.013, Medcalc Software Ltd) was used for statistical analysis14.

Results

Primary bariatric surgery was performed on 253 patients between January 2020 and September 2022; 35 patients were excluded due to incomplete follow-up, 18 for specific urological contraindications (see urological counseling session). After two years of follow-up, 185 patients (47 ± 12 years, 38 males, and 147 females) were included in the study; 114 of them received Sleeve Gastrectomy (SG), 30 received One-Anastomosis Gastric Bypass (OAGB), and 41 underwent Roux-n-Y Gastric Bypass (RYGB) (Table 1).

Table 1 Study population characteristics.
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Patients underwent urine analysis and provided early morning urine samples before the nutritional assessment. 25 patients (13.5%) found crystalluria in their samples, evaluated for the presence of urinary stones. Most of the urine crystals were found as calcium oxalate (n = 19) followed by uric acid (n = 4) and amorphous phosphate/urate (n = 2). Urinary ph modification was assessed for each bariatric procedure reporting a slightly statistically not significant acidification (Table 2). None of these 25 patients resulted symptomatic during the urological examination, referring to no episode of fever nor flank pain. Subsequently, all those patients were invited to perform a low-dose abdominal CT scan without contrast. Kidney stone disease was described in 12 patients (6.49%. HU range + 400 + 1100) out of the 25 with crystalluria (Fig.  1).Most of the patients (n = 10) showed a monolateral single kidney stone located in the inferior calyces with a maximum diameter inferior to 6 mm and no caliectasis nor hydroureteronephrosis. Only two patients showed monolateral multiple kidney stone disease affecting both middle and inferior calices without any alteration of the urinary tracts and with a maximum stone diameter inferior to 7 mm. No simultaneous cases of ureteral stones were reported. These 12 patients belonged to the group where calcium oxalate crystals were discovered during the urine analysis.

Table 2 Urinary Ph modification for each bariatric procedure. P significance was set at p < 0.05.
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These patients were all female and had a mean age, BMI, and %EWL of 46.7 years, 28.14 (kg/m2), and 63.5%, respectively. The average water intake was 1.12 L/day and each patient assumed supplementation. Out of these, 12 patients, 2 underwent RYGB, 2 OAGB, and 8 SG. These findings highlight variations in the occurrence of crystals and stones across different surgical interventions, suggesting differential effectiveness or patient characteristics between groups.

A comprehensive statistical analysis did not show any statistically significant association between the incidence of stones and crystals and the type of surgical intervention (P > 0.05 for all correlations). The results are explained by the small number of stones and crystals accounted for in our population study. The analysis of incidences of conditions such as HTN, Dyslipidemia (DLP), Obstructive Sleep Apnea Syndrome (OSAS), and T2DM across three surgical intervention groups revealed significant differences in the incidence rates of HTN, DLP, and OSAS among the groups, as evidenced by p-values of 0.0144, 0.0207, and approximately 0.00000016, respectively. These findings indicate a variation in health condition prevalence after surgical intervention, highlighting potentially differential health impacts of the interventions. Conversely, T2DM did not show a significant difference in incidence rates across the groups, with a p-value of 0.2733, suggesting a consistent prevalence regardless of surgical intervention type (Table 3).

Table 3 Characteristics of patients with kidney stone disease.
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Analyzing the incidence of crystals and stones development according to BMI post-treatment, with a new threshold of < 30 and > = 30 kg/m2, provides the following insights:

For Crystals Post-Bariatric Surgery:

  • Proportion with Condition: Of the group < 30 BMI, approximately 12.14% of individuals developed crystals post-treatment, compared to 17.02% in the > = 30 BMI group.

  • Confidence Intervals: For the group < 30, the confidence interval ranges from 6.73 to 17.55%, and 6.28–27.77% for the > = 30 group.

  • P-Value: 0.547 indicates that the difference in the proportion of individuals developing crystals between the two BMI post-treatment categories is not statistically significant.

For Stones Post- Bariatric Surgery:

  • Proportion with Condition: Approximately 3.57% of individuals in the < 30 BMI group developed stones post-treatment, compared to 14.89% in the > = 30 group.

  • Confidence Intervals: For the < 30 group, the confidence interval ranges from 0.50 to 6.65%, and 4.72–25.07% for the > = 30 group.

  • P-Value: 0.017 indicates a statistically significant difference in the incidence of stone development between the two BMI post-treatment categories. This suggests a higher occurrence in individuals with a BMI > = 30 post-treatment.

The analysis shows a significant difference in the incidence of stone development based on BMI post-treatment, with a higher incidence observed in individuals with a BMI > = 30. For crystals, the difference doesn’t achieve statistical significance (Fig. 2).

Fig. 2
figure 2

Proportion of conditions by BMI post-treatment category.

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Discussion

BS is an effective treatment for morbid obesity. It results in rapid, pronounced, and sustained weight loss, improved quality of life, and prolonged life expectancy. Obesity-related diseases, such as T2DM, HTN, OSAS, and DLP, typically improve or even resolve after BS.

Despite benefits, some proportion of operated patients experiences long-term complications, post-bariatric procedure, such as nutritional deficiencies, gallbladder lithiasis, recurrent calcium oxalate urolithiasis, and osteoporosis9,10.

The literature shows the highest risk of developing kidney stones is reported in malabsorptive procedures, the intermediate in RYGB, and the lowest in restrictive techniques11,12. However, Laurens et al., in their study, indicate that the incidence of kidney stones after primary BS procedures was increased more than six-fold compared to matched controls from the normal population. The highest incidence was observed after malabsorptive procedures, while RYGB and SG had similar incidences13. Recently, Ghanem et al. in a comprehensive review about BS impact on organ transplant, stated that RYGB portends up to a threefold increase in calcium oxalate stone formation postoperatively affecting graft survival15. In our study, kidney stone disease was described in 12 patients (6.49%), and most of them underwent SG without statistical significance compared with the other bariatric procedures, probably for unbalanced group analysis (114 SG vs. 30 OAGB vs. 41 RYGB).

Nephrolithiasis develops from urinary metabolic changes in these patients, such as low urinary volume, hypocitraturia, and hyperoxaluria. Our study found calcium oxalate stones in every patient. The underlying mechanisms for increased urinary oxalates in post-BS patients have not been completely elucidated but may be related to dietary factors, intestinal fat malabsorption, and changes in intestinal oxalate transport. A diet rich in oxalate and/or poor in calcium decreases the generation of unabsorbable calcium oxalate complexes, resulting in a higher amount of free oxalate in the intestinal lumen. Vitamin C supplements are metabolized to oxalate contributing to hyperoxaluria.

Urine crystals are a marker indicating urine supersaturation, which may cause stone formation due to an imbalance in inhibitors and promoters of urolithiasis16. According to Daudon et al., crystalluria can monitor patients with metabolic disorders affected by urinary stone disease17. Based on the literature, calcium oxalate is the most common type of crystalluria18. Even though the type of urine crystals does not always correlate with that of the stones, several studies suggest that calcium oxalate crystals highly predict the presence of calcium oxalate stones16,19. Although in our study, patients affected by kidney stone diseases did not require surgical interventions, and so no stone analysis was performed, the presence of calcium oxalate crystals may suggest that the majority of the stone’s composition may be made of calcium oxalate, which is the most common type of stone discovered in bariatric patients.

After bariatric surgery, a diet rich in oxalate and poor in calcium is very common and linked to a reduction in the assumption of milk and other dairy products because the intake of these foods is associated with gastrointestinal symptoms and “dumping syndrome” in some patients9.

As known by the literature, changing solubility and supersaturation of the solutes is a crucial factor in lithogenesis. Most bariatric surgery patients have low fluid intake due to the small gastric pouch; although patients are advised to an appropriate fluid intake to achieve a urinary volume of approximately 2.5 L/day, patients in our study took 1.12 L/ day of water. These data suggest that an inadequate fluid and calcium intake, may have a crucial role in the pathogenesis of urinary stone disease. The results indicate that BC and different bariatric procedures, EWL, and comorbidities didn’t represent a risk factor affecting the stone incidence (supporting nutritional counseling as crucial in risk prevention). However, patients BMI at the end of the procedure significantly affects stones appearance. Of the group, 3.57% of individuals in the BMI < 30 group developed stones post-treatment, compared to 14.89% in the > = 30 group, which confirmed that obesity is the central risk factor for stone development, while crystalluria depends more on dietary habits.

Specific guidelines to prevent nephrolithiasis after BS are lacking, but reducing oxalate intake, avoiding gram doses of vitamin C supplementation, and increasing calcium and fluid intake should be recommended.

Postoperative bariatric follow-up is crucial for weight loss support and early detection of nutritional deficiencies, urolithiasis, and osteoporosis. Medium-long follow-up can be used to observe relatively unknown long-term complications of bariatric surgery.

Despite several limitations, such as a short observation period, limited sample size, and no control group, our findings suggest that patients undergoing bariatric surgery may develop kidney stone disease regardless of surgical procedure, particularly in those remaining in the obesity BMI class. Pre- and post-operative counseling should include a discussion about the risk of developing this complication for patients who are considering bariatric surgery. After surgery, even in absence of symptoms, a 24-hour urinary calcium and oxalate measurements and an abdominal ultrasound to evaluate the upper urinary tract could be indicated as follow-up prevention strategy.

Conclusions

Despite its benefits, bariatric surgery may lead to long-term complications, including, in some experiences, an increased risk of kidney stones; in our survey, 6.49% of patients (% like those reported in worldwide population) presented with lithiasis without correlation with bariatric surgery (any operation).

Post-bariatric surgery, dietary evaluation is crucial in treating and preventing stone formation. Following surgery, monitoring urinary stones could be indicated particularly for patients who remain in the obesity category.