DOI: 10.1542/peds.2013-2103; originally published online March 24, 2014;Pediatrics

Ning Li, Xuefeng Zhou, Jiyan Yuan, Guiying Chen, Hongliang Jiang and Wen ZhangCeftriaxone and Acute Renal Failure in Children

  

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Ceftriaxone and Acute Renal Failure in Children

WHAT’S KNOWN ON THIS SUBJECT: Ceftriaxone at therapeuticdoses can lead to renal stone formation.

WHAT THIS STUDY ADDS: Renal stone formation with ceftriaxonetherapy can result in postrenal acute renal failure in children. Thecondition can be treated effectively by timely pharmacotherapy orretrograde ureteral catheterization with good prognosis.

abstractOBJECTIVE: Our aim was to evaluate the clinical profile, treatment,and outcome of ceftriaxone-associated postrenal acute renal failure(PARF) in children.

METHODS: We retrospectively studied 31 consecutive cases from 2003to 2012 for PARF after ceftriaxone treatment. There was no past historyof urolithiasis or nephropathy in these children.

RESULTS: The average time of ceftriaxone administration before PARFwas 5.2 days. The major symptoms apart from anuria included flankpain (.3 years old, 25/25), excessive crying (,3 years, 6/6), andvomiting (19/33). Ultrasound showed mild hydronephrosis (25/31)and ureteric calculi (11/31). Nine children recovered after 1 to 4days of pharmacotherapy. Twenty-one children who were resistantto pharmacotherapy underwent retrograde ureteral catheterization.After catheterization of their ureters, normal urine flow wasobserved, and the symptoms subsided immediately. Catheterinsertion failed in 1 child who subsequently underwent 3 sessionsof hemodialysis before normal urination was restored. Ceftriaxonewas verified to be the main component of the calculi in 4 children bytandem mass spectrometric analysis. The recovery was complete inall cases.

CONCLUSIONS: Ceftriaxone therapy in children may cause PARF. Earlydiagnosis and prompt pharmacological therapy are important in re-lieving the condition. Retrograde ureteral catheterization is an effectivetreatment of those who fail to respond to pharmacotherapy. Pediatrics2014;133:e917–e922

AUTHORS: Ning Li, MD,a Xuefeng Zhou, MD,a Jiyan Yuan,MD,a Guiying Chen, MD,b Hongliang Jiang, MD,b and WenZhang, MDa

aDepartment of Pediatric Surgery, Tongji Hospital, Tongji MedicalCollege, and bTongji School of Pharmacy, Huazhong University ofScience and Technology, Wuhan, China

KEY WORDSacute renal failure, child, ceftriaxone

ABBREVIATIONSPARF—postrenal acute renal failureRUC—retrograde ureteral catheterizationTMS—tandem mass spectrometric

Dr Li collected the data and wrote the article; Profs Zhou andYuan performed the treatment of the children; Dr Chen and ProfJiang carried out the ceftriaxone detection by massspectrometric analysis; Prof Zhang conceptualized the article;and all authors approved the final manuscript as submitted.

www.pediatrics.org/cgi/doi/10.1542/peds.2013-2103

doi:10.1542/peds.2013-2103

Accepted for publication Jan 14, 2014

Address correspondence to Wen Zhang, MD, Department ofPediatric Surgery, Tongji Hospital, Tongji Medical College,Huazhong University of Science and Technology, No 1095 JiefangRd, Tongji Hospital, Wuhan 430030, China. E-mail:wenzhang09@126.com

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2014 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors have indicated they haveno financial relationships relevant to this article to disclose.

FUNDING: No external funding.

POTENTIAL CONFLICT OF INTEREST: The authors have indicatedthey have no potential conflicts of interest to disclose.

PEDIATRICS Volume 133, Number 4, April 2014 e917

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Ceftriaxone is a third-generation ceph-alosporin that is widely used to treatvarious infections during childhood.Long plasma half-life and single dailydose are the main advantages of thisagent. Approximately 33% to 67% ofceftriaxone is excreted unmetabolizedin the urine, whereas the remainder isexcreted through biliary elimination.1

Clinical studies have demonstratedthat ceftriaxone can cause biliarypseudolithiasis,2,3 nephrolithiasis,4–7

and bladder sludge,8 especially inchildren.

Ceftriaxone at therapeutic doses canlead to crystallization in the urine andthese crystals adhere to the surface ofrenal tubularcells.5Severenephrolithiasiscan cause postrenal acute renal failure(PARF). To date there are only a fewstudies reporting on PARF associatedwith ceftriaxone.9–11

Our aim was to study the clinical fea-tures, treatment, and outcome ofceftriaxone-associated PARF in chil-dren.

METHODS

Between January 1, 2003 and June 30,2012, of the 127 PARF children admittedto the Pediatric Surgery Department ofTongji Hospital, there were 31 childrenwho had a history of ceftriaxone ad-ministration a few days before PARF.These children were identified as sub-jects for the study. The history of cef-triaxone treatment was verified frompatient records in 9 children andreportedbyparents in the remaining22children.

The diagnosis of PARF was based onsudden onset of anuria, flank pain, andrenal percussion pain associated withelevated serum creatinine and/or se-rumurea nitrogen in a childwhohadnopast history of urolithiasis. The renalultrasonography findings includednormal-sized kidneys, the presence orabsence of hydronephrosis, or ureteric

calculi with no renal vascular abnor-mality or thrombus. The children whohad known pre-renal causes of ARF,glomerulonephritis, or disorders thatcan cause renal injury such as auto-immune diseases, malignant hyperten-sion, nephrotoxic drugs, rhabdomyolysis,or disseminated intravascular coagula-tion, etc, were excluded from the study.

The medical records of these 31 chil-dren were retrospectively reviewed forthe following data: primary disease forwhich ceftriaxone was administered;dose and time of ceftriaxone adminis-tration; time from the ceftriaxoneadministration to PARF; clinical mani-festation of PARF; concomitant symp-toms; renal ultrasound findings; tandemmass spectrometric (TMS) analysis ofstones; treatment methods; and timetaken for resolution of PARF. Prognosisdata were also reviewed.

The beginning of PARF was consideredtobe fromthe last spontaneousvoiding.Treatment time of PARF was consideredto be from the beginning of treatmentuntil the reflow of urine (at a rate of.0.5 mL/kg/h).

The therapeutic principle adopted in-cluded initiation of pharmacotherapyand, if the children showed no sign ofurination until serum creatinineexceeded 500 mmol/L, treatment withretrograde ureteral catheterization(RUC) was performed. In cases inwhich both methods failed, hemodial-ysis was used. Nephrostomy was con-sidered as the last option. Parentswere told to follow-up at least 1 monthafter discharge.

Pharmacotherapy included spasmolysis(anisodamine), alkalization (sodiumbicarbonate), antibiotics, albuminsupplement, and low doses of dexa-methasone. Total liquid intake wasstrictly controlled and monitored. Po-tassium supplementation was not usedunless polyuria stage was reached.Serum creatinine, blood potassium,blood pressure, and evidence for

pulmonary edema were monitored ac-cordingly.

RESULTS

Baseline Characteristics, PrimaryDiseases, and CeftriaxoneAdministration

Among the 31 cases of ceftriaxone-associated PARF, 23 were boys and 8were girls. The mean age was 5.1 years(range, 1–12 years). The primarydiseases for which ceftriaxone wasadministered included 12 cases ofpneumonia, 5 cases of upper respi-ratory tract infections, 5 cases of si-nusitis, 1 case each of meningitis,parotitis, and left arm trauma, and 6postoperative cases (3 for hypospa-dias, 2 for appendicitis, and 1 for fem-oral fracture). Family histories revealeda history of urolithiasis in parents of 3cases. None of the siblings had urinarycalculi.

The average time of ceftriaxone ad-ministration was 5.2 days (range, 3–7days). The exact doses of ceftriaxoneadministration were available in 13 casesand ranged from 70 to 100 mg/kg/d(mean, 86.7 mg/kg/d). The average timefrom the first day of ceftriaxone ad-ministration to anuria was 5.4 days(range, 3–9 days).

Clinical Features

The clinical symptoms included a sud-den onset of anuria for at least 24 hours(31/31),flank pain (.3 years old, 25/25;17 bilateral and 8 unilateral), excessivecrying (,3 years, 6/6), and nauseaand/or vomiting (19/31). Nine childrenhad mild dehydration and 5 wereedematous. Severe dehydration wasnot recorded in any case.

Renal ultrasonography revealed bilat-eral mild hydronephrosis in 6 childrenand unilateral mild hydronephrosis in19 children. Six children had normalrenal ultrasonographs. The averageanteroposterior diameter of the pelvis

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was 0.64 cm (range, 0.4–1.2 cm). Ure-teric calculi were found in 11 children.The diameters of calculi ranged from0.2 to 0.6 cm (mean, 0.3 cm). Biliaryultrasonography was performed in 22children, among which 4 were found tohave biliary pseudolithiasis. Abdominalradiographs showed fluid levels in 3cases and no calculus was observed inany of the patients (Table 1).

Treatment and Effectiveness

Nine patients began to urinate and re-covered after 1 to 4 days of pharma-cotherapy.

Twenty-onechildrenwhowereresistantto pharmacotherapy and had serumcreatinine .500 mmol/L required RUCby cystoscopy. Five children had serumcreatinine levels above 500 mmol/L atthe time of admission. Sixteen children(mean age, 4.46 2.0 years) underwentbilateral RUC, and 5 children (meanage, 8.2 6 2.9 years) underwent uni-lateral RUC. Unilateral RUC was used inthese 5 children as only 1 side could becatheterized; a catheter could not beinserted into the other side owing to anedema of the ureterovesical orifice andcalculi blockage. These 5 children werealso significantly older than the other16 children (P , .01). Once the cathe-ters were in situ, normal urinationreturned and the situation improvedaccordingly in children who underwentbilateral and unilateral catheterization.The catheters were removed after 3 to5 days.

RUC failed on both sides in 1 patient,a 10-year-old boy, owing to dense calculiblocking the ureteic orifices. Afterseveral attempts to catheterize thepatient, the orifices of the ureter be-came edematous and started to bleed.This child was referred for hemodialy-sis. After 3 sessions of hemodialysis onalternative days, normal urination wasre-established.

The mean treatment duration was 1.8days (range, 1–7 days). The mean

anuria period was 3.1 days (range, 1–8days). No nephrostomy was performedin any of the cases. The serum creati-nine and serum urea nitrogen de-creased rapidly after urinationreturned. Urinalysis of samples col-lected soon after recovery variedwidely. Most children had red bloodcells and white blood cells in the urine,especially those who underwent RUC.Proteinuria wasmild or absent. Hyalineand granular casts were observed ina few patients. Subsequent urinalysis 1to 5 days later revealed normal find-ings except for a few white blood cellsin a few cases. The ultrasonographyfindings did not help to choose themodality of treatment, whether con-servative line or ureteral catheteriza-tion.

All childrenwerecuredanddischarged.Twenty-three children were followedover thenext 4weeks.Nosignof relapsewas observed. Ultrasound scans, per-formed1monthpost-discharge, showedno signs of stones. Four children hadmild hydronephrosis and required fur-ther follow-up with regular ultrasoundexamination.

TMS Analysis

Because of its sand-like structure, mostof the calculi were flushed away duringthe catheterization. We could only col-lect 6 samples of urinary calculi and in 4of themceftriaxonewasconfirmedtobethe main component of the calculi byTMS (Fig 1). The other 2 samples weretoo heavily contaminated with redblood cell fragments to be of any valuefor analysis.

DISCUSSION

Several studies have shown ceftriaxoneto cause biliary pseudolithiasis2,3 andnephrolithiasis.4–7 However, ceftriaxone-associated PARF9–11 has been rarelyreported. In this study we identified31 children who had PARF who had

a definite history of ceftriaxone treat-ment demonstrating the causal role ofceftriaxone in PARF.

Ceftriaxone at therapeutic doses cancrystallizewith calcium in the urine andadhere to the surface of renal tubularcells.5 It can even increase urinarycalcium excretion.12 Thus ceftriaxone,by increasing the excretion of urinarycalcium and crystallizing with calcium,forms stones that obstruct the ureters,resulting in PARF. In addition, the “re-flex anuria” mechanism also contrib-utes to this situation.13,14 We observedthrough the use of ultrasonographythat the majority of cases (25/31) hadno detectable abnormality at least in 1kidney. In 5 cases, unilateral RUC re-solved the anuria, and when unilateralureter drainage was established thecontralateral obstruction improvedimmediately whether the contralateralside had hydronephrosis or uretericcalculi. These observations support thereflex anuria mechanism. The ob-struction of the ureter on 1 side byceftriaxone crystals led to reflex anuriaon the other side, resulting in PARF.However the exact mechanism of reflexanuria is still unknown. Dehydrationmay be an important inducing factor.Most of the children in this series werereluctant to drink much water after theprimary disease, which may have ex-acerbated the pathogenesis.

Although ultrasonography is a highlyspecific modality in PARF diagnosis, notall PARF patients show positiveresults.15 Six children in the currentstudy did not show abnormalities inrenal sonography. Sudden and com-plete anuria in these children with nocontributing history or specific labo-ratory findings for other causes led usto confirm PARF in these children.

Generally the ceftriaxone renal stonesare small, remain asymptomatic, anddo not need any specific treatment.4,6,7

After cessation of ceftriaxone therapy,the stones vanish by themselves. With

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TABLE1

Characteristicsof

31ChildrenWho

HadCeftriaxone-AssociatedPARF

No.

Gender

Age,y

Ceftriaxone

Doses,

mg/kg/d

Days

ofCeftriaxone

Treatm

ent

TimeFrom

Ceftriaxone

Administration

toPARF,d

Anuria

FlankPain

orCrying

Vomiting

Hydronephrosis,cm

UretericCalculi,cm

OtherClinical

Findings

Treatm

ent

1M

8—

55

√√

Right0.5

RightR

UC2

M2

82.6

44

√√

√Left0.4

Left0.2

Pharmacotherapy

3F

3—

44

√√

Left0.7

BilateralRUC

4M

5—

54

√√

Left0.8,right0.6

BilateralRUC

5M

12—

33

√√

√Left0.6,right0.8

Right0.4

RightR

UC6

M2

87.0

54

√√

√Left0.4

Left0.2

Pharmacotherapy

7M

788.9

44

√√

√Left0.9,right0.5

Left0.2

Fluidlevel

BilateralRUC

8M

495.5

33

√√

Right0.6

Right0.3

BilateralRUC

9M

796.6

66

√√

Left0.6,right0.8

Biliarypseudolithiasis

BilateralRUC

10F

1—

66

√√

√Right0.4

BilateralRUC

11M

8—

57

√√

Pharmacotherapy

12M

6—

79

√√

BilateralRUC

13F

6—

45

√√

Right0.5

BilateralRUC

14M

1083.1

45

√√

√Left1.0,right0.4

Left0.4

Hemodialysis

15F

3—

66

√√

√Right0.4

BilateralRUC

16M

7—

78

√√

√Left0.6

Biliarypseudolithiasis

BilateralRUC

17M

1—

77

√√

√Left0.4

BilateralRUC

18M

3—

76

√√

√Pharmacotherapy

19M

586.3

66

√√

√Left0.8

BilateralRUC

20M

4—

55

√√

√Right0.6

Right0.3

Fluidlevel

LeftRU

C21

M7

—5

5√

√Right1.0

Pharmacotherapy

22F

284.7

45

√√

Pharmacotherapy

23F

370.4

55

√√

√BilateralRUC

24M

496.8

78

√√

√Right0.7

Right0.2

Fluidlevel

Pharmacotherapy

25M

4—

55

√√

√Right0.4

BilateralRUC

26M

9—

45

√√

√Left0.6,right1.2

Right0.6

LeftRU

C27

F5

—5

5√

√Left0.5

Left0.2

Biliarypseudolithiasis

Pharmacotherapy

28M

8100

76

√√

√Right0.9

LeftRU

C29

F3

73.5

44

√√

BilateralRUC

30M

6—

75

√√

√Left0.8

Left0.3

Biliarypseudolithiasis

BilateralRUC

31M

282.0

66

√√

√Right0.5

Pharmacotherapy

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this view, we initiated pharmacother-apy for all children upon diagnosis, and9 children responded well. In the otherchildren, the ceftriaxone stones werefound to be more compact andobstructed the urinary tract. Theirureteral orifices had inflammatoryswelling under cystoscopy, whichmight have aggravated the obstruction.Pharmacotherapy aimed to dilate theureters and relieve spasm (anisodamine),relieve edema of the renal pelvisand ureter (albumin and low dose ofdexamethasone), and most importantly,prevent complications such as acidosis(sodium bicarbonate) and urinarytract infections (antibiotics). Oncethe ceftriaxone administration isstopped, swelling of the ureteral ori-fices subsides, and stones get expelled,thus relieving the symptoms. Thepharmacotherapy helps to maintainthe homeostasis during this waitingperiod. Through pharmacotherapy usealone, 9 children in this study recovered

by days 1 to 4. Theoretically, pharma-cotherapy can be continued as long asthe water-electrolyte and acid-basebalance is not severely disturbed. Inthis study, the longest pharmacother-apy lasted 4 days.

Acute pulmonary edema resulting fromfluid retention and cardiac arrestresulting from hyperkalemia are 2 ofthe most lethal complications of PARF.For this reason we paid special atten-tion to restriction of fluids and avoidedpotassium supplements until the poly-uria stage. Through these measuresneither pulmonary edema nor hyper-kalemia was observed. The earliest andmost prominent abnormality in routineblood tests that was observed was in-creasing creatinine levels. We set theserumcreatinine toa level not toexceed500 mmol/L, above which catheteriza-tion was performed.

For those patientswho showed no signof recovery after pharmacotherapy

and increasingserumcreatinine levelsbeyond 500 mmol/L, RUC was per-formed. Viewed through the cysto-scope, the ceftriaxone calculiappeared as sand grains. Because ofthe sand-grain nature of this calculi,ultrasonic lithotripsy, holmium laserlithotripsy, or lithotomy do not renderany help. In the majority of cases thecatheters could be inserted into theblocked ureters without much diffi-culty. Through catheterization alonethe stones could be flushed out insome instances. In a few cases, how-ever, the stones were more compact,which made it difficult to insert thecatheters. The catheterization failedoften in older children. All childrenyounger than 4 years had easy cath-eterization. The mean age of the 5children in whom catheterizationfailed on 1 side was 8.2 years. Bilateralcatheterization of the ureter failed onboth sides in 1 patient, a 10-year-oldchild. It appears that more and stablecrystallization is needed to obstructthe urinary tract in older children.Hence, the stone formation is lower inolder children, but once it forms, thestones are usually more compact.

All children in this study had a goodpost-treatment prognosis. Four chil-dren were found to have mild hydro-nephrosis after 1 month. This might bebecause the hydronephrosis caused bythe obstruction had not yet recovered.The other reason could be previousexistence of other urinary abnormali-ties, such as ureteropelvic junctionobstruction, which increases the riskfor nephrolithiasis.16 No other signifi-cant sequelae were observed in anycase. These results indicate thatceftriaxone-associated PARF is re-versible and has a good prognosis ifprompt and proper treatments areadministered in time.

The limitations of the current studyinclude small sample size and retro-spective design. The non-availability of

FIGURE 1StoneanalysisbyTMS.Urinarysedimentsamples fromapatientwerewashedanddissolved in1%formicacid solution. Ceftriaxone calciumdissolved in 1% formic acid solutionwasusedas apositive control. ABSciex 4000 Q-Trap instrument was used for TMS analysis. The Q1 scan showed ceftriaxone parent ionwithmass charge ratio 553.0 in both A, control and C, patient sample. Product ion scans further showedthat in theB, controlandD, patient sample, the fragment ions (fragmentof ceftriaxone)weresimilar. Cps,counts per second; Da, dalton; m/z, mass charge ratio.

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exact doses of ceftriaxone in all cases isanother limitation. TMS analysis ofstones confirmed ceftriaxone as themain component of the calculi in only4 patients. The sand-grain nature ofceftriaxone stones makes it difficultto collect. This particular limitation ofthe study stresses the need for an im-proved technique for the collectionand analysis of these calculi in futurestudies.

Based on the current data it is difficultto estimate the incidence of PARF in allceftriaxone-treated children. We pre-sumethat it is low. If anuriaorflankpainis observed in children receiving cef-triaxone treatment, therapy should bestopped immediately and such childrenshould be investigated by using therelevant blood tests and renal ultra-sonography. If PARF is confirmed, thenthe drug should be stopped and proper

therapy for PARF should be initiated atthe earliest.

CONCLUSIONS

This retrospective study showed thatceftriaxone therapy could lead to PARF.In ceftriaxone-associated PARF, con-servative pharmacotherapy is helpful,but when it fails, RUC is an effectivetherapeutic option.

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DOI: 10.1542/peds.2013-2103; originally published online March 24, 2014;Pediatrics

Ning Li, Xuefeng Zhou, Jiyan Yuan, Guiying Chen, Hongliang Jiang and Wen ZhangCeftriaxone and Acute Renal Failure in Children

  

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