Abstract
BACKGROUND:
Acute gastroenteritis (AGE) can cause acute kidney injury (AKI) via hypoperfusion mechanisms. Early detection of AKI caused by AGE can significantly decrease mortality rates. In Saudi Arabia, studies investigating the association between AGE and AKI are limited; thus, we aimed to fill this knowledge gap.
OBJECTIVES:
Analyze all cases of AGE reported in tertiary-care hospitals to assess the prevalence of AKI among AGE patients.
DESIGN:
Retrospective cohort
SETTINGS:
Single tertiary-care center
PATIENTS AND METHODS:
The study included patients treated for AGE between October 2017 and October 2022. Stool culture was used to diagnose AGE. Inclusion criteria were infective diarrhea and/ or vomiting, and availability of data (demographics, comorbidities, malignancies, length of hospital stay, vital signs at the time of diagnosis, dehydration, causative agents of diarrhea, hemodialysis status, and laboratory data.
MAIN OUTCOME MEASURES:
Prevalence of AKI among AGE patients and factors associated with development of AKI.
SAMPLE SIZE:
300 patients diagnosed with AGE.
RESULTS:
Of the 300 patients with AGE, 41 (13.6%) had AKI, those older than 60 years were more likely to develop AKI. The most frequent cause of AGE was Salmonella spp. (n=163, 53.3%), whereas AKI was most common in Clostridium difficile AGE patients (n=21, 51.2%). Furthermore, the most common comorbidity in the present study was malignancy, especially leukemia and lymphoma the risk of AKI was independently associated with mild dehydration, higher serum urea concentrations and low GFR values.
CONCLUSIONS:
Patients hospitalized for diarrheal disease are at an increased risk of developing AKI due to dehydration and comorbid conditions. It is crucial to keep kidney function in mind for AGE patients as this is associated with a high mortality rate and poor prognosis.
LIMITATIONS:
The main limitation of this study was its retrospective design. Another limitation is that it is limited to a single center.
CONFLICTS OF INTEREST:
None.
INTRODUCTION
Acute gastroenteritis (AGE) is characterized by rapid onset of diarrhea, which may be accompanied by vomiting, nausea, or fever, that usually lasts less than 14 days.1 In the United States (US) alone, approximately 179 million episodes of AGE occur each year, resulting in approximately 600 000 hospitalizations and 5000 deaths.2 Clinically, gastroenteritis can manifest as mild, moderate, or severe disease with the main symptoms of abdominal pain, diarrhea, nausea, and vomiting. A severe form of AGE includes bloody stools, fever, and sepsis.3–5 AGE is usually diagnosed clinically based on the clinical history, physical examination, and evaluation of risk factors. The diagnosis can be supported based on the results of a complete blood count (CBC), basic metabolic panel, stool analysis and culture, and serum electrolyte levels.6,7
Most AGE cases are caused by viruses. Bacterial AGE accounts for approximately 20% of cases. Viral gastroenteritis usually affects children aged <2 years, whereas bacterial gastroenteritis occurs more often in those who are older than 2 years. However, diarrhea that lasts for at least 14 days is most frequently caused by parasitic infections.8,9 Rotavirus is the most common cause of severe AGE in children and is responsible for an estimated 527 000 deaths in children younger than 5 years of age.10 Although AGE usually remits spontaneously and only requires minimal medical intervention, severe complications, such as dehydration, may result in prolonged vomiting and diarrhea.
Dehydration occurs when the body loses a lot of water, electrolytes as well as other fluids; thus, an increase in serum osmolality of greater than 294 mOsm/kg is considered dehydration.11 Dehydration is classified into three stages: mild, moderate, and severe. The assessment of the severity of dehydration in children is as follows: mild, 3–5% of dehydration; moderate, 6–9% of dehydration; and severe, more than 10% of dehydration. The percentage of dehydration is determined through physical findings and vital signs.12 In adults, mild dehydration is defined as a water loss equal to 1% of the body weight, which may result in headache, weakness, dizziness, and lethargy. Moderate dehydration can result in a dry mouth, low urinary output, tachycardia, and loss of skin elasticity. The body cannot regulate its temperature and blood pressure in case of severe dehydration. Patients with mild-to-moderate dehydration should receive oral rehydration therapy as first-line treatment.13,14
Acute kidney injury (AKI) is not an individual disease entity, but rather, is a syndrome that is characterized by a group of symptoms that occur together. AKI is a consequence of several underlying conditions; 20% of hospitalized patients have AKI, and 10% of these patients require renal replacement therapy.15,16 According to the latest Kidney Disease Improving Global Outcomes (KDIGO) clinical guideline for the classification and management of AKI, an increase in serum creatinine (SCr) by ≥0.3 mg/dL within 48 hours and to ≥1.5 times the baseline level over 7 days or decreased urinary output <0.5 mL/kg/h for 6–12 hours indicates AKI.17
AGE may result in AKI via a prerenal mechanism (hypoperfusion). Thus, hospitalized children and adults with gastroenteritis who develop AKI are more likely to have a longer hospital stay as well as a higher risk of chronic kidney disease (CKD) in the long term.18,19 AKI is a multifactorial illness because of the multiple etiopathogenic mechanisms.20 For example, chemotherapeutic agents may cause multiple forms of AKI by damaging all kidney compartments.21 A study conducted in the United States showed that only 0.8% of patients with infectious gastroenteritis developed AKI,22 whereas another study conducted in Italy showed a high incidence of AKI (approximately 24%) in patients with AGE.23
Milder forms of AKI can lead to a two-fold increase in the risk for CKD, which makes early detection an important strategy to prevent complications.23,24 Thus, studying the complications and association between AKI and AGE would improve the understanding of AGE-related AKI. This study aimed to determine the prevalence and evaluate the association between AKI and AGE in both the adult and pediatric populations at our institution.
PATIENTS AND METHODS
This retrospective chart review was conducted in King Abdulaziz Medical City, Jeddah, Saudi Arabia. No consent was required as no identities were revealed and the study was approved (approval no. NRJ22J-068-03) by the Institutional Review Board of the King Abdullah International Medical Research Center. The main objective of this study was to evaluate the association between AGE and AKI. In this study, AGE was confirmed using stool culture, whereas the diagnosis of AKI was based on the KDIGO criteria. The Chronic Kidney Disease Epidemiology Collaboration equation (CKDEPI) was used to calculate the estimated glomerular filtration rate (eGFR) for patients who were older than 17 years, whereas the revised bedside Schwartz formula was used to calculate the eGFR for children (age 1–17 years). Dehydration was classified into three stages: mild, moderate, and severe, based on the clinical assessment, which included the buccal mucosa, eyes, and skin. Vital signs, such as heart rate, respiration, and blood pressure, were used to assess the severity of dehydration. A consecutive sampling technique was used to include all patients who fulfilled the criteria until a sample size similar to that in other studies was achieved. The study cohort included 300 patients who were diagnosed with AGE during a 5-year period (from October 2017 to October 2022). The inclusion criteria were infective diarrhea and/or vomiting, availability of data on creatinine levels, and a diagnosis of AGE in the discharge summary. The exclusion criteria were any pathological conditions other than infections that were associated with diarrhea, chronic diarrhea, genetic syndromes, absence of data on serum creatinine values, and chronic renal impairment. Data collection was performed in a single step by reviewing and collecting information from the electronic records of patient files at the study institution. We analyzed the following data: demographics, comorbidities (DM, HTN, malignancies, etc.), length of hospital stay (days), patients’ vital signs at the time of diagnosis, dehydration, causative agents of diarrhea, hemodialysis status, and laboratory data (serum creatinine, serum blood urea nitrogen [BUN], serum potassium, and serum sodium).
Statistical analysis
Data analysis was performed using RStudio (version 4.1.1) (R Foundation for Statistical Computing, R version 4.0.1, Vienna, Austria, and the dplyr package). Numerical data are presented as mean and standard deviation (SD) or median (interquartile range), whereas categorical data are expressed as frequency and percentage. The prevalence of AKI was assessed using a one-sample proportion test with continuity correction, and the prevalence was expressed as the effect estimate along with the respective 95% confidence interval (95% CI). Factors associated with AKI were analyzed using univariate tests, including the Fisher exact test or the Pearson chi-square test for categorical variables, and with the Wilcoxon rank sum test for numerical variables. Factors that showed a significant association in the univariate analysis were then entered into a binomial logistic regression analysis. The results of the regression analysis were expressed as odds ratios (OR) and 95% CIs. Statistical significance was set at P value <.05.
RESULTS
Data from a 5-year period (from October 2017 to October 2022) for 300 participants were analyzed. Of these participants, 160 (53.3%) were male, and less than half (42.7%) of the patients were younger than 18 years. The median (25th–75th percentile) age of adults was 56 (43–65) years. The median (IQR) height of adults was 154.0 (52.5) cm and the median weight was 56.0 (60.5) kg. Malignancies were the most common type of comorbidity (46.7%), followed by hypertension (24.0%) and diabetes mellitus (22.3%). The other clinical characteristics are summarized in (Table 1).
Table 1.
Demographic and clinical characteristics.
| Parameter | Overall (n=300) | Missing (%) | Acute kidney injury | P value | |
|---|---|---|---|---|---|
| No (n=259) | Yes (n=41) | ||||
| Age, years | |||||
| ≤18 | 128 (42.7) | 0 | 126 (48.6) | 2 (4.9) | <.001 |
| >18 to 30 | 15 (5.0) | 15 (5.8) | 0 | ||
| >30 to 45 | 33 (11.0) | 26 (10.0) | 7 (17.1) | ||
| >45 to 60 | 57 (19.0) | 44 (17.0) | 13 (31.7) | ||
| >60 | 67 (22.3) | 48 (18.5) | 19 (46.3) | ||
| Sex | |||||
| Male | 160 (53.3) | 0 | 139 (53.7) | 21 (51.2) | .770 |
| Female | 140 (46.7) | 120 (46.3) | 20 (48.8) | ||
| Height (cm) | 151 (54) | 0 | 150 (60) | 160 (17) | <.001 |
| Weight (kg) | 51.0 (57.0) | 2 (0.7) | 45.1 (31.9) | 70.7 (22.8) | <.001 |
| Comorbidities | |||||
| Diabetes mellitus | 67 (22.3) | 0 | 44 (17.0) | 23 (56.1) | <.0001 |
| Hypertension | 72 (24.0) | 0 | 47 (18.1) | 25 (61.0) | <.0001 |
| Malignancies | 140 (46.7) | 0 | 120 (46.3) | 20 (48.8) | .77 |
| Length of hospital stay (days) | 6.0 (7) | 0 | 6.0 (7) | 8.0 (8) | .0786 |
| Heart rate (beats/min) | 108.2 (26.2) | 6 (2.0) | 110.1 (26.4) | 96.1 (21.4) | .002 |
| Systolic BP (mmHg) | 114.6 (18.8) | 4 (1.3) | 113.5 (17.7) | 121.9 (23.9) | .057 |
| Diastolic BP (mmHg) | 67.8 (21.9) | 4 (1.3) | 67.9 (22.6) | 66.9 (16.7) | .641 |
Data are n (%).
In general, 41 patients (13.7%; 95%CI, 10.1%–18.2%) had AKI; 21 of 41 patients developed AKI mainly due to AGE, whereas 20 patients had malignancy as a comorbidity, which indicates that AKI had a multifactorial causation (chemotherapy + AGE). Twenty patients developed AKI, whereas 21 patients with Clostridium difficile infection were suspected to have a hospital-acquired infection. Significantly higher proportions of patients with AKI were >45 to 60 years of age (31.7% vs. 17.0% without AKI) and >60 years of age (46.3% vs. 18.5% without AKI, respectively; P<.0001).
Additionally, patients with AKI had significantly higher body weight (Figure 1) and height, and slower heart rate than those without AKI (Table 2). The length of stay (LOS) for patients with AGE who experienced AKI was longer than for patients without AKI. This result demonstrated that both spent a significant amount of time in the hospital because the majority of patients also had cancer. On the other hand, the length of hospitalization in patients who develop AKI during AGE without cancer as a comorbidity was 8.5 days, compared to 6.5 days for patients with AGE without both AKI and cancer. The proportion of patients with diabetes mellitus (56.1% vs. 17.0%, P<.0001) and hypertension (61.0% vs. 18.1%, P<.0001) was significantly higher among patients with AKI than in those without AKI but the difference was not statistically significant (Table 1).
Figure 1.
Body weight by the presence of acute kidney injury (P<.001).
Table 2.
Gastrointestinal and kidney-related variables of the participants.
| Parameter | Overall (n=300) | Missing | Acute kidney injury | P value | |
|---|---|---|---|---|---|
| No (n=259) | Yes (n=41) | ||||
| Symptoms | |||||
| Fever | 136 (45.3) | 0 | 120 (46.3) | 16 (39.0) | .382 |
| Vomiting | 114 (38.0) | 0 | 98 (37.8) | 16 (39.0) | .884 |
| Diarrhea | 299 (99.7) | 0 | 258 (99.6) | 41 (100.0) | .999 |
| Frequency of diarrhea, per day | |||||
| <4 | 170 (56.7) | 0 | 151 (58.3) | 6 (14.7) | .039 |
| 4–6 | 83 (27.7) | 71 (27.4) | 12 (29.3) | ||
| 7–10 | 29 (9.7) | 20 (7.7) | 19 (46.3) | ||
| >10 | 18 (6.0) | 17 (6.6) | 4 (9.7) | ||
| Dehydration | |||||
| No dehydration | 193 (64.3) | 0 | 179 (69.1) | 0 | <.001 |
| Mild | 71 (23.7) | 58 (22.4) | 20 (48.7) | ||
| Moderate | 30 (10.0) | 20 (7.7) | 17 (41.4) | ||
| Severe | 6 (2.0) | 2 (0.8) | 4 (9.9) | ||
| Causative agent | |||||
| Salmonella | 163 (54.3) | 0 | 148 (57.1) | 15 (36.6) | .026 |
| C difficile | 100 (33.3) | 79 (30.5) | 21 (51.2) | ||
| Others | 37 (12.3) | 32 (12.4) | 5 (12.2) | ||
| Hemodialysis | |||||
| Not used | 298 (99.3) | 0 | 259 (100) | 39 (95.1) | .009 |
| Used | 2 (0.7) | 0 | 2 (4.9) | ||
| Laboratory parametersa | |||||
| Serum urea (mmol/L) | 4.6 (4.7) | 2 (0.7) | 3.7 (3.3) | 10.1 (7.3) | <.001 |
| Serum potassium (mmol/L) | 4.4 (7.6) | 0 | 3.9 (0.7) | 7.6 (20.4) | .264 |
| Serum sodium (mmol/L) | 134.7 (11.2) | 0 | 135.5 (4.0) | 129.2 (28.4) | .063 |
| Creatinine (μmol/L) | 68.7 (58.2) | 0 | 54.3 (32.0) | 159.0 (94.8) | <.001 |
| eGFR (mL/min/1.73 m2) | 93.8 (73.4) | 0 | 101.0 (75.8) | 48.9 (28.8) | <.001 |
Data are expressed as mean (standard deviation) or as frequency (percentage).
Diarrhea was the most commonly reported gastrointestinal symptom among the participants (99.7%), followed by fever (45.3%) and vomiting (38.0%). The most common frequency of diarrhea among patients with AGE-induced AKI was 7–10 times per day (46.3%, n=19), followed by 4–6 times per day (29.3%, n=12). Dehydration was reported in 107 (35.7%) participants. Mild dehydration (48.7%, n=20) was the most common subcategory among participants with AGE-induced AKI. The frequency of diarrhea (P=.039) and dehydration (P<.0001) differed significantly in patients with AKI. Furthermore, a significantly higher proportion of patients with AKI had gastroenteritis caused by C difficile (51.2%) than those who did not have AKI (30.5%; P=.026).
Hemodialysis was performed in only two patients (4.9%, n=2). A significantly higher proportion of patients with AKI did not need renal replacement therapy (95.1%, n=39). The serum urea concentrations were lower than in those without AKI (P<.0001) and the serum creatinine was higher in those with AKI (P<.0001) (Table 2).
The most common cause of AGE was Salmonella (54.3%), followed by C difficile (33.3%) and rotavirus (4.7%). The remaining patients had positive blood cultures for other microorganisms, as shown in (Figure 2). The independent risk factors for AKI were assessed by incorporating significantly associated factors from univariate analysis into a multivariate regression model (Table 3). Consequently, assumption tests were done to exclude any variable that violates the assumptions of multicollinearity (variance inflation factor [VIF] >5). The variables were patients’ age (VIF=20.2) and frequency of diarrhea (VIF=5.5). Results revealed that the risk of AKI was independently associated with having mild dehydration, higher serum urea concentrations and low GFR values.
Figure 2.
Causative agents of acute gastroenteritis in 300 patients from October 2017 to October 2022.
Table 3.
Results of the logistic regression analysis of risk factors for acute kidney injury among patients with gastroenteritis.
| Parameter | Odds ratio | 95% CI | P value |
|---|---|---|---|
| Height (cm) | 1.04 | 1.00–1.08 | .060 |
| Weight (kg) | 1.00 | 0.97–1.03 | .988 |
| Diabetes mellitus | |||
| No | Reference | ||
| Yes | 1.14 | 0.28–4.59 | .854 |
| Hypertension | |||
| No | Reference | ||
| Yes | 2.55 | 0.60–11.3 | .206 |
| Heart rate (beats/min) | 0.99 | 0.97–1.02 | .641 |
| Dehydration | |||
| No dehydration | Reference | ||
| Mild | 4.04 | 1.14–15.0 | .031 |
| Moderate | 4.52 | 0.78–29.0 | .098 |
| Severe | 49.6 | 0.82–2,722 | .056 |
| Causative agent | |||
| Salmonella | Reference | ||
| C difficile | 1.48 | 0.44–5.04 | .522 |
| Others | 1.39 | 0.20–7.83 | .721 |
| Hemodialysis | |||
| Not used | Reference | ||
| Used for <3 months | NA | NA | .993 |
| Used for >3 months | 0.06 | 0.00–2.37 | .190 |
| Urea (mmol/L) | 1.15 | 1.01–1.29 | .018 |
| Creatinine (μmol/L) | 1.00 | 0.98–1.02 | .926 |
| Glomerular filtration rate (estimated) (mL/min/1.73 m2) | 0.96 | 0.93–0.99 | .011 |
NA, not applicable, because the variable contains zero frequency. Model fit statistics: deviance 108, R squared McFadden’s 0.547, R squared Nagelkerke 0.643, overall: chi-square 131, df 11, P<.001.
A few laboratory tests were performed on the sample, including serum potassium, sodium, urea, and creatinine. The median serum potassium and sodium levels in patients with age-related AKI were 4.0 and 134.0 mmol/L, respectively. In this study, C difficile was the primary bacterium that resulted in poor prognosis, and increased the serum urea as high as 8.5 mmol/L and creatinine to 130 µmol/L, and decreased GFR to 41.0 mL/min). Furthermore, Salmonella was the second most common bacterium that resulted in poor outcomes (serum urea 7.9, creatinine 152.0, and GFR 50.0) (Table 4).
Table 4.
Laboratory results of patients with acute kidney injury.
| Parameter | Overall (n=41) | Causative agent | P value | ||
|---|---|---|---|---|---|
| Salmonella (n=15) | C difficile (n=21) | Others (n=5) | |||
| Serum potassium (mmol/L) | 4.0 (3.2–4.9) | 4.0 (3.2–4.6) | 4.1 (3.5–4.9) | 4.2 (3.1–5.1) | .869 |
| Serum sodium (mmol/L) | 134.0 (132.0–138.0) | 133.0 (132.0–134.0) | 135.0 (131.0–139.0) | 137.0 (133.0–140.0) | .211 |
| Serum urea (mmol/L) | 8.4 (6.1–12.2) | 7.9 (5.8–14.3) | 8.5 (6.7–11.6) | 6.1 (4.8–19.5) | .858 |
| Serum creatinine (μmol/L) | 141.0 (84.0–194.0) | 152.0 (83.5–235.0) | 130.0 (86.0–186.0) | 144.0 (126.0–168.0) | .870 |
| Glomerular filtration rate (estimated) (mL/min/1.73 m2) | 44.0 (26.0–60.0) | 50.0 (27.5–60.0) | 41.0 (26.0–64.0) | 44.0 (30.0–49.0) | .976 |
Data are presented for the overall subpopulation and stratified by the causative agent. Data are expressed as median (IQR).
DISCUSSION
In the present study, 300 patients met the inclusion criteria, and male patients were more likely to develop AGE (53.3%). However, there was no sex-specific predisposition for AGE-related AKI. A previous study in Italy that included 114 patients over a 2-year period had nearly the same male-to-female ratio during as in this study.23
This is the first study that involved both children and adults who were hospitalized for AGE, and 13.6% of AGE patients developed AKI; however, a study by Bradshaw found that only 1% of children with infectious diarrhea developed AKI. Their findings revealed a very different prevalence from that identified in this study. Most of our patients who developed AKI during AGE were older than 60 years, which explains the variation between this study’s results and that of Bradshaw, which only involved the pediatric population.22 Another study by Marzullo et al revealed that 24.6% of their pediatric patients developed AKI.23 Their findings proved that AKI might develop in any age group, either pediatric or adult. Another study conducted at Mulago National Referral Hospital in Kampala, Uganda, from June 2007 to August 2010, found a high prevalence of AKI among AGE patients. The study included 422 patients, and 169 (40%) of them had AKI.25 Another study revealed a high prevalence of AKI in 82% of pediatric patients.26 The discrepancy between our findings and those of the previous two studies is due to their populations being from underdeveloped nations, which means that they had more severe dehydration due to the difficulties in accessing medical treatment.
AGE is a significant contributor to acute renal damage and can be avoided. There is a high risk of AKI when diarrheal fluid loss is not adequately or promptly restored. Many studies have shown that AGE is the leading cause of AKI.25,27 Most of the patients in this study who developed AKI had mild dehydration (n=20, 48.7%). The findings of this study are consistent with those of Marzullo et.al; that is, most patients with AKI had mild dehydration (n=27, 96.4%). This finding indicates that kidney injury can be induced by mild dehydration and not only by severe dehydration. Both studies showed that dehydration is one of the primary mechanisms that leads to AKI; thus, it is essential to look out for symptoms of dehydration in patients with AGE. In addition to the creatinine level, the early indicators of AKI in this study were dehydration, high urea, hyperkalemia, and hyponatremia. In contrast, Marzullo et al revealed that dehydration and serum bicarbonate levels were significant indicators of AKI.23
In patients with AKI, the serum urea and serum creatinine levels are essential indicators of prognosis, as high levels are associated with significant complications. The most common comorbidity in the present study was malignancy, specifically leukemia and lymphoma, as half of the patient population who developed AKI had hematological malignancy as a comorbidity. This finding was similar to that of Bradshaw et al, who reported that patients with rheumatologic and hematologic conditions were at a higher risk of developing AKI.22
In patients with Salmonella, the AKI prevalence was 36.5% (15 out of 41). Moreover, the prevalence of AKI was 51.2% (21 of 41) among patients with C difficile infection. In one study conducted in the western region of Saudi Arabia, the prevalence of C difficile was 9.1% during the 2 years from October 2018 to October 2020; antibiotic use was the most common risk factor associated with C difficile infection. However, the percentage of AKI in the population was not studied because of poor renal status at baseline before the C difficile infection. Moreover, the authors reported 28.4% of hypotension and 17.2% of shock among patients with diarrheal illnesses due to C difficile.28 Our center includes a large oncology center (Princess Norah Oncology Center, Jeddah, Saudi Arabia), and as the vast majority of oncology patients receive antibiotics, it is not unusual to encounter large numbers of C difficile infections.
The most common organism that resulted in AKI was rotavirus 33.3% (11 out of 33 in Marzullo et al), followed by Salmonella 16.7% (1 out of 6).23 As a result of the small number of newborn patients in the current study, we did not diagnose many rotavirus infections. Our study found that the infectious organism interferes with the prevalence of AKI, with a positive stool culture of C difficile or Salmonella being more likely to be associated with AKI. In contrast, the study by Marzullo et al showed that infectious agents did not influence the prevalence of AKI.23
The main limitation of this study was its retrospective design. Another limitation is that it was limited to a single center. In this context, the accumulated data from additional centers nationwide will provide health authorities with an opportunity to improve the elements that have a negative impact on outcomes.
In conclusion, in the current study, 13.6% of patients experienced AKI during AGE. Patients who were older than 60 years were more likely to develop AKI. The most offending organism that causes AGE is Salmonella, whereas the causative agent that results in AKI is C difficile. The leading indicators of AKI in patients who were hospitalized for gastroenteritis are serum urea and dehydration. It is essential to pay attention to kidney function in patients with AGE because devolving AKI will result in a poor prognosis as well as a high mortality rate.
Funding Statement
None.
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