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URO0010.1177/2051415814556335Journal of Clinical UrologyNandwani et al.

Original Article

Metabolic abnormalities in patients treated with percutaneous nephrolithotomy

Journal of Clinical Urology 1­–9 © British Association of Urological Surgeons 2015 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/2051415814556335 uro.sagepub.com

GM Nandwani, J Stoves, MF Azhar, CI Pereni and T Shah

Abstract Objectives: To assess metabolic abnormalities in patients with percutaneous nephrolithotomy (PCNL) that could pose a risk for stone recurrence. Materials and methods: The data was collected retrospectively on all patients who had PCNL and metabolic studies, between January 2000 and September 2012. Results: There were 144 patients; median age and follow up were 49.5 (15– 4) years and 80.2 (16–180) months, respectively. Nearly half of the patients had staghorn calculus. Metabolic abnormalities (MAs) were found in 55 (38.2%). The 31 (21.5%) of these had multiple metabolic abnormalities (MMA) while 24 (16.6%) had a single metabolic abnormality (SMA). Uricosuria was found in 24 (16.6%), hyperoxaluria in 22 (15.3%), hyperphosphaturia in 18 (12.5%), hypercalciuria in 10 (7%), hypomagnesuria in 6 (4.2%), cystinuria in 5 (3.5%) and hypocitraturia in 5 (3.5%). Hyperuricaemia was present in 10 (7%), hypercalcaemia in 5 (3.5%), hyperphosphataemia in 7 (5%) and renal tubular acidosis in 1 (0.7%). In nonstaghorn, MAs were found in 25 (35.2%) and 16 (64%) of these had MMA. In patients with staghorn, MAs were present in 30 (41%) patients. Half of the patients 15 (50%) in this group had MMA. A high proportion of the first time stone formers requiring surgical treatment had MAs and 57% of these had MMA. Stone analysis was available for 69 (48%) and 37 (53.6%) of these had mixed composition. The highest proportion of patients with uric acid stones had MA 89% followed by cystine stones 80%, matrix stones 50%, calcium oxalate 36.6%, carbonate apatite 36.4% and triple phosphate 33.3% . Conclusion: A high proportion of first time stone formers, staghorn and non-staghorn stone formers with PCNL had MA. These findings suggest that the treatment of metabolic abnormalities can play an important role in reducing the risk of stone recurrences and management may include referral to dedicated metabolic stone clinics. Keywords Metabolic abnormalities, percutaneous nephrolithotomy, chemical abnormalities, metabolic screen Date received: 13 July 2014; accepted: 24 September 2014

Introduction Percutaneous nephrolithotomy (PCNL) is considered a gold standard minimally invasive procedure for removal of the large renal stones with overall stone-free rates ranging between 75.7% and 83.5% and relatively low complication rates.1,2 PCNL is superior to Shock Wave Lithotripsy (SWL) and ureteroscopy for large stone burden.3,4 Stone recurrence rates of 22.6% to 36.8% have been reported after PCNL. There is a higher risk of stone recurrence in patients with residual fragments, infective stones and structural abnormalities of the

urinary tract.5–7 These recurrences reduce patient’s quality of life and may also increase the economic burden placed on health care systems. Bradford Teaching Hospital NHS Foundation Trust, Bradford, UK Corresponding author: Tariq Shah, The Yorkshire Clinic, Bradford Road, Bingley, West Yorkshire, BD16 1TW, UK. Email: [email protected]

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It has also been shown that rates of stone recurrence after SWL and PCNL are higher in patients with metabolic abnormalities (MAs).8 We conducted a retrospective study to assess the frequency of metabolic abnormalities that could pose a risk for stone recurrences in patients who were treated with PCNL.

Table 1.  Reference laboratory values in 24 hour urine at Bradford Teaching Hospital. Male

Female

Hypercalciuria

>7.5 mmol/d

>9 mmol/d

Hyperuricosuria

>4.5 mmol/d

>3.9 mmol/d

Materials and methods

Hyperoxaluria

>0.49 mmol/d

>0.32 mmol/d

Study design is a retrospective clinical cohort study: the notes were reviewed of all patients who had PCNL and metabolic study, between January 2000 and September 2012, for the diagnosis of any risk factors, which may increase the chances of stone recurrences. Included in the study were all patients who had completed a metabolic stone screening (MSS) and had PCNL as a treatment for the stone. MSS was done either prior to PCNL and/or at least 6 weeks after stone clearance. For MSS we measured serum creatinine, urea, sodium, potassium, calcium, phosphate, urate, chloride and bicarbonate in a peripheral blood sample. Single 24 hours urine was collected in a bottle containing 75 ml of 2.5N HCl. The standard written instructions were given to the patients and they were advised not to change their dietary habits. Patients who had incomplete 24 hour urine collection based on 24 hour urinary creatinine were excluded from the study (22 mmol/d

Hypocitraturia

2.6 mmol/l

Hyperuricaemia

>430 μmol/l

>380 μmol/l

Hyperphosphataemia

>1.5 mmol/l

>1.5 mmol/l

patients received general dietary stone prevention advice and those who were diagnosed to have a metabolic abnormality were also followed up in a dedicated metabolic stone clinic to optimise the management of MAs. Fisher’s exact test was used to measure statistical significance among various groups with MAs. A p value 25) was present in 20 (14%) and median BMI was 28.8 (26–35.5) while the median stone burden was 792 (28.3–6022) mm2. There were 55 (38.2%) patients with MAs. Multiple metabolic abnormalities (MMA) were detected in 31 (21.5%) while 24 (16.6%) had solitary metabolic abnormality (SMA). MA in urine was found in 35 (24.3%), 5 (3.5%) had MA in blood while 15 (10.4%) had MA in both blood and urine. Uricosuria was found in 24 (16.6%), hyperoxaluria in 22 (15.3%), hyperphosphaturia in 18 (12.5%), hypercalciuria in 10 (7%), hypomagnesuria in 6 (4.2%), cystinuria in 5 (3.5%) and hypocitraturia in 5 (3.5%). Hyperuricaemia was present in 10 (7%), hypercalcaemia in 5 (3.5%), hyperphosphataemia in 7 (5%) and renal tubular acidosis in 1 (0.7%). Higher proportions of these abnormalities were present as a part of MMA (Figure 1).

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Nandwani et al. The most common combination in MMA were uricosuria with oxaluria in 12 (8.3%), oxaluria with hyperphosphaturia in 11 (7.6%), uricosuria with hyperphosphaturia in 10 (7%) and hypercalciuria with uricosuria in 6 (4.2%). For further details please see Table 3. Table 2.  Characteristics of patients who underwent PCNL. Total patients

144

  •  Age (yrs)

49.5 (15–84)

  •  Male : Female   •  Follow up (months)   • Comorbidities

77 (53.5%) : 67 (46.5%) 80.2 (16–180)  

 Hypertension    

44 (30.5%)

 Diabetes    

23 (16%)

  Coronary artery disease    

21 (15%)

 COPD    

11 (8%)

 CKD    

10 (7.6%)

  •  Previous stone treatment

79 (55%)

  •  Stone characteristics



 Non-staghorn    

71 (49.3%)

 Staghorn    

73 (50.7%)

 Complete      

37 (25.7%)

      Partial

36 (25%)

There were 79 (55%) patients with previous stone disease and MAs were found in 27 (34.2%). There were 12 (44.4%) with SMA and 15 (55.5%) with MMA. The commonest abnormalities in this group were hyperoxaluria 14 (18%), hyperphosphaturia 13 (16.4%) and uricosuria 10 (12.6%). The first time stone former group comprised of 65 (45%) patients. MAs were found in 28 (43%) and MMA were seen in 16 (57%). The commonest abnormalities were uricosuria 14 (21.5%), hyperoxaluria 8 (12.3%), hypercalciuria 7 (11%) and hyperuricaemia 6 (9.2%). There was a difference in types of the commonest abnormalities between these two groups but results did not reach statistical significance (Figure 2). Non-staghorn and staghorn stones were present in 71 (49.3%) and 73 (50.7%), respectively. In nonstaghorn, MAs were found in 25 (35.2%) and 16 (64%) of these had MMA. In patients with staghorn, MAs were present in 30 (41%) patients and 15 (50%) had MMA. In both groups the common MAs were uricosuria, hyperoxaluria and hyperphosphaturia and there was no significant difference in MAs between these groups (Figure 3). Stone analysis was available for 69 (48%) and 37 (53.6%) of these had mixed composition. MAs were found in 31 (45%) patients with stone analysis. MMA and SMA were seen in 15 (22%) and 16 (23%) patients, respectively. The most common stones were calcium oxalate stones 30 (43%) followed by carbonate apatite 11 (16%), triple phosphate 9 (13%) and uric acid 9 (13%) (Table 4). Majority of the mixed compositions comprised of calcium oxalate/ calcium carbonate appetite in 11 (16%), Carbonate appetite/ calcium phosphate 4 (6%) and triple phosphate/ calcium carbonate appetite 7 (10%).

Figure 1.  Metabolic abnormalities in PCNL patients (n = 144) (Uric = uricosuria, Oxal = hyperoxaluria, PO4ur = hyperphosphaturia, Calciur = hypercalciuria, Cystinur = cystinuria, Hypocit = hypocitraturia, HypoMag = hypomagnesuria, HyperUric = hyperuricaemia, HyperCal = hypercalcaemia, HyperPO4 = hyperphosphataemia, RTA = renal tubular acidosis].

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Table 3.  Combination of abnormalities in blood and urine (total MMA = 31). n

%

  •  Calciuria + phosphaturia + oxaluria

1

1.8%

  •  Calciuria + phosphaturia + oxaluria + hypercalcaemia

1

1.8%

  •  Calciuria + uricosuria + phosphaturia + oxaluria

1

1.8%

  •  Calciuria + uricosuria + phosphaturia + oxaluria + hypercalcaemia

1

1.8%

  •  Calciuria + uricosuria

3

5.35%

  •  Calciuria + uricosuria + phosphaturia

1

1.8%

  •  Calciuria + oxaluria

1

1.8%

  •  Uricosuria + phosphaturia + oxaluria

4

7.14%

  •  Uricosuria + phosphaturia + hyperuricaemia

1

1.8%

  •  Uricosuria + oxaluria

2

3.57%

  •  Uricosuria + cystinuria + oxaluria + hyperuricaemia

1

1.8%

  •  Uricosuria + hyperuricaemia

2

3.57%

  •  Uricosuria + hypomagnesuria

1

1.8%

  •  Uricosuria + oxaluria + hyperphosphataemia

1

1.8%

  •  Uricosuria + hyperphosphataemia

1

1.8%

  •  Phosphaturia + hyperphosphataemia

1

1.8%

  •  Phosphaturia + oxaluria + hyperuricaemia

1

1.8%

  •  Oxaluria + hypercalcaemia

1

1.8%

  •  Oxaluria + hypocitraturia

1

1.8%

  •  Hypocitraturia + hypomagnesuria + hypercalcaemia + hyperuricaemia

1

1.8%

  •  Hypocitraturia + hypomagnesuria + hyperuricaemia

1

1.8%

  •  Hypomagnesuria + hyperuricaemia + hyperphosphataemia

1

1.8%

  •  Hypomagnesuria + RTA

1

1.8%

  •  Hypercalcaemia + hyperphosphataemia

1

1.8%

The highest proportion of patients with MAs had uric acid stones (89%) followed by cystine stones (80%) and matrix stones (50%). MAs in calcium oxalate, carbonate apatite and triple phosphate stones were present in 36.6%, 36.4% and 33.3%. Uricosuria (44.4%) was predominant in uric acid stones followed by hyperuricaemia 33.3%, hypocitraturia 22.2% and hypomagnesuria 22.2%. Triple phosphate stones predominantly had hyperoxaluria (22.2%). Hyperoxaluria and hyperphosphaturia were dominant in calcium oxalate stones while 60% of cystine stones had pure cystinuria (Tables 4 and 5). The stone recurrence 13 (23.6%) was slightly higher in patients with MAs in comparison to 17 (19%) without MA

(p = 0.5). There were 97 (67.4%) in the stone-free category and 38 (39.2%) had MAs. We did not find significant difference in stone recurrences in stone-free patients with or without MAs, 7 (18.4%) and 13 (20%), respectively (p = 0.7). However, higher numbers of patients with MAs and residual fragments, 6 (35.3%), had stone recurrences vs. 4 (13.3%) without MA and residual fragments (p = 0.13). The overall median time to recurrence of stones for patients with MAs and without MAs was 21.5 (5–120) and 24 (6–132) months, respectively. The median time to recurrence with RF in patients with MAs and without MAs were 18 (6–120) and 55.5 (12–132) months, respectively. But these results did not reach statistical significance.

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Nandwani et al.

Figure 2.  Metabolic abnormalities with and without previous stone disease (Uric = uricosuria, Oxal = hyperoxaluria, PO4ur = hyperphosphaturia, Calciur = hypercalciuria, Cystinur = cystinuria, Hypocit = hypocitraturia, HypoMag = hypomagnesuria, HyperUric = hyperuricaemia, HyperCal = hypercalcaemia, HyperPO4 = hyperphosphataemia, RTA = renal tubular acidosis).

Figure 3.  Metabolic abnormalities in non-staghorn and staghorn patients (Uric = uricosuria, Oxal = hyperoxaluria, PO4ur = hyperphosphaturia, Calciur = hypercalciuria, Cystinur = cystinuria, Hypocit = hypocitraturia, HypoMag = hypomagnesuria, HyperUric = hyperuricaemia, HyperCal = hypercalcaemia, HyperPO4 = hyperphosphataemia, RTA = renal tubular acidosis).

Discussion Metabolic assessment has previously been reserved for patients with recurrent stone disease such as; multiple stones, bilateral stones, stones in paediatric age group, patients with bowel disease and surgery or in patients with known metabolic abnormalities.10,11

In recent studies, frequencies of MAs have shown variability that may be related to geographical or populationrelated factors.12–14 In our study MA were found in a 38.2% of those undergoing PCNL. MMA were found in high proportion of patients 56.3% who had MAs. A study on patients with SWL found hypercalciuria, hyperuricosuria,

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9 (13.0%)

11 (16.0%)

5 (7.2%)

2 (3.0%)

2 (3.0%)

1 (1.4%)

Carbonate apatite  

Cystine  

Matrix  

2,3-Dihydroxyadenine

Calcium phosphate

9 (13.0%)

Triple phosphate (struvite)  

Uric acid  

30 (43.4%)

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SMA = Nil MMA = 1 (100%)

1 (50%)

SMA = 3 (75%) MMA = 1 (25%)

4 (80%)

SMA = 2 (50%) MMA = 2 (50%)

4 (36.4%)

SMA = 4 (50%) MMA = 4 (50%)

8 (89%)

SMA = 1 (33.3%) MMA = 2 (66.6%)

3 (33.3%)

SMA = 4 (44.4%) MMA = 6 (6.6%)

11 (36.6%)

1 (2.6%)

2 (5.2%)

1 (2.6%)

3 (8%)

7 (18.4%)

6 (15.7%)

5 (13.1%)

13 (34.2%)

No. (%)

No. (%)

MA No. (%)

Staghorn = 38

Overall stones = 69

Calcium oxalate  

Stone analysis





SMA = Nil MMA = 1 (100%)

1(100%)

SMA = 3 (100%) MMA = Nil

3 (100%)

SMA = 1 (50%) MMA = 1 (50%)

2 (28.5%)

SMA = 3 (60%) MMA = 2 (40%)

5 (83.3%)

SMA = 1 (50%) MMA = 1 (50%)

2 (40%)

SMA = 3 (60%) MMA = 2 (40%)

4 (30.7%)

MA No. (%)

Table 4.  Results of stone analysis and the commonest metabolic abnormalities associated with type of stones. Total = 69 (48%).





1 (2.6%)

2 (6.4%)

4 (13%)

3 (10%)

4 (13%)

17 (55%)

No. (%)

Non-staghorn = 31









SMA = Nil MMA = 1 (100%)

1(50%)

SMA = 1 (50%) MMA = 1 (50%)

2 (50%)

SMA = 1 (33.3%) MMA = 2 (66.6%)

3 (100%)

SMA = 0 MMA = 1 (100%)

1 (25%)

SMA = 4 (66.6%) MMA = 3 (33.3%)

6 (35.3%)

MA No. (%)

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Nandwani et al. Table 5.  Results of stone analysis and the commonest metabolic abnormalities associated with type of stones. Total = 69 (48%). Overall (60)

Staghorn (38)

Non-staghorn (31)

Stone analysis

Type of metabolic abnormalities

No. (%)

No. (%)

No. (%)

Calcium oxalate

Hyperoxaluria

3 (10%)

3 (23%)





Hyperphosphataemia

3 (10%)

1 (7.6%)

2 (11.8%)



Uricosuria

2 (6.6%)

1 (7.6%)

1 (5.8%)



Hypocitraturia

2 (6.6%)

1 (7.6%)

1 (5.8%)



Hypomagnesuria

1 (3.3%)



1 (5.8%)



Hyperphosphaturia

2 (6.6%)

1 (7.6%)

1 (5.8%)



Hypercalcaemia

1 (3.3%)



1 (5.8%)



Hyperuricaemia

1 (3.3%)



1 (5.8%)

Triple phosphate (struvite)

Hyperoxaluria

2 (22.2%)

1 (20%)

1 (25%)



Hyperuricaemia

1 (11%)

1 (20%)





Uricosuria

1 (11%)

1 (20%)





Hypercalciuria

1 (11%)

1 (20%)





Hyperphosphataemia

1 (11%)

1 (20%)



Uric acid

Uricosuria

4 (44.4%)

3 (50%)

1 (33.3%)



Hyperuricaemia

3 (33.3%)

2 (33.3%)

1 (33.3%)



Hypocitraturia

2 (22.2%)

2 (33.3%)





Hypomagnesuria

2 (22.2%)

1 (16.6%)

1 (33.3%)



Hyperphosphataemia

2 (22.2%)

1 (16.6%)

1 (33.3%)



Hyperoxaluria

1 (11%)



1 (33.3%)



Hypercalcaemia

1 (11%)

1 (16.6%)





Hypercalciuria

1 (11%)



1 (33.3%)

Carbonate apatite

Hypercalciuria

2 (18.2%)



2 (50%)



Uricosuria

2 (18.2%)

1 (14.3%)

1 (25%)



Hypomagnesuria

1 (9%)

1 (14.3%)





Hyperoxaluria

1 (9%)

1 (14.3%)





Hyperphosphaturia

1 (9%)







RTA

1 (9%)

1 (14.3%)



Cystine

Cystinuria

3 (60%)

3 (100%)





Hyperoxaluria

1 (20%)



1 (33.3%)



Hyperphosphaturia

1 (20%)



1 (33.3%)



Uricosuria

1 (20%)



1 (33.3%) (Continued)

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Table 5. (Continued) Overall (60)

Staghorn (38)

Non-staghorn (31)

Matrix

Hyperoxaluria

1 (50%)

1 (100%)





Hyperphosphaturia

1 (50%)

1 (100%)





Hypercalciuria

1 (50%)

1 (100%)



2,3-Dihydroxyadenine

NAD







Calcium phosphate

NAD







hyperoxaluria and hypocitraturia in 31%, 12%, 18% and 27% of patients, respectively.15 In a review by Park and Pearle,16 hypercalciuria was found in 35% to 65% patients with nephrolithiasis. In our cohort the predominant abnormalities were hyperuricosuria 16.6%, hyperoxaluria 15.3%, hyperphosphaturia 12.5% and hypercalciuria 8%. These differences could be due to selective patient group in our study and in addition may be related to geographical, ethnic origin and dietary factors. It is controversial whether metabolic assessment in first time stone former is cost effective. In recent studies it was found that an almost equal proportion of patients with or without recurrent stone disease had Mas.14,17 Our study also showed similar results but importantly a high proportion of the first time stone formers requiring PCNL had MAs and 57% of these had MMA. Uricosuria was the commonest abnormality followed by hyperoxaluria, hyperphosphaturia, hypercalciuria and hyperuricaemia. Studies have also shown that stone recurrences after PCNL in patients with MAs can be reduced with initiation of targeted medical treatment.18,19 Akagashi et al. studied characteristics of 82 patients with complete staghorn calculi and metabolic evaluation was available in only 37 (45%).20 Hyperuricaemia, cystinuria and hypercalciuria were found in 14.6%, 2.4% and 37.8%, respectively. There were 38 patients with complete staghorn in our study and severe disability was noted in 2 (5.4%), morbid obesity in 5 (13.5%) and 3 (8%) had gout and thyroid disorder. The predominant abnormality was hyperoxaluria in 7 (19%) followed by uricosuria in 5 (13.5%). Hyperuricaemia, hypocitraturia and cystinuria were present in each of 3 (8%). The differences in MAs could be due to dietary habits, obesity and heterogeneous ethnic population in our catchment area. Their group had large number of patient with moderate to severe disability 13.4%, indwelling catheter 8.5% and UTI 24.4%. Not surprisingly they had large number of struvite stones (32%), whereas in our study there were only 13% of struvite stones. Eighty percent of their group had calcium containing stones (struvite 32.1%, calcium oxalate (CaOx) 13.6%, CaPO4 10% and CaOx+CaPO4 18%). This could explain the high percentage of hypercalciuria.

Moreover, they had metabolic evaluation in 37 (45%) which can create a selection bias. Amaro et al. assessed MAs in 22 of 37 patients with staghorn stones.21 They studied only those patients whose GFR was >60 ml/min and found metabolic abnormalities in 68.2%. The most common was hypercalciuria in 9 (64.2%) followed by hypocitraturia in 8 (53.3%). Hyperuricosuria and hypomagnesuria were found in 21.4% and 14.2%, respectively, while hyperoxaluria, primary hyperthyroidism and RTA were found in 7.1% of patients. Probably the reasons for the differences in results from our study could be due to vastly different patient group, co-morbidities, ethnic origin and possibly dietary habits. In non-staghorn patients MA were found in 49.3% and the commonest MA were uricosuria in 10 (14%), hyperoxaluria in 9 (12.7%), hyperphosphaturia in 9 (12.7%) and hypercalciuria in 7 (10%). Our study showed different MA in comparison to the above mentioned studies but importantly half of these had MMA. Also, trend for finding MA in the non-staghorn stone patients was nearly same. These suggest that the management of MA may decrease the risk of stone recurrence in either group. We also compared relationship of MA with the type of stones. The highest proportion of patients with uric acid stones had MA 89% followed by cystine stones 80%. Uricosuria (44.4%) was predominant in uric acid stones followed by hyperuricaemia 33.3%, hypocitraturia 33.3% and hypomagnesuria 33.3%. Triple phosphate predominantly had hyperoxaluria (22.2%). Hyperoxaluria and hyperphosphaturia were dominant in calcium oxalate stones while 60% of cystine stones had pure cystinuria (Tables 4 and 5). The limitations of our study were small study cohort and retrospective study design. However, it showed higher number of patients had MA and stone recurrences were higher in patients with MAs with shorter time to recurrence particularly in patients with residual stone fragments. The statistical significance was not achieved may be due to small sample size. These results suggest large number of patients may get benefit by managing in dedicated metabolic stone clinics and may get reduction in future stone recurrences.

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Conclusions Metabolic abnormalities were found in high proportion of patients who were treated with PCNL. Uricosuria, hyperoxaluria, hyperphosphaturia and hypercalciuria were found in high proportion of patients. In many cases multiple metabolic abnormalities were identified and abnormalities were also found in large proportion of first time stone formers. The highest frequencies of metabolic abnormalities were associated with uric acid and cystine stones. These findings suggest that the treatment of metabolic abnormalities can play an important role in reducing the risk of stone recurrences, and management may include referral to a dedicated metabolic stone clinic with specific management advice. Conflicting interests The authors declare that there is no conflict of interest.

Funding None declared.

Ethical approval Not applicable.

Guarantor TS.

Contributorship TS conceived the study. TS, JS and GMN were involved in research of the literature, data collection, data analysis and the initial drafts of the manuscript. GMN wrote the final draft and analysed data edited by TS. All authors reviewed and edited the manuscript and approved the final version of the manuscript.

Acknowledgements None.

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