Impact of Reporting Gram Stain Results from Blood Culture Bottles on the Selection of Antimicrobial Agents

Yuki Uehara, MD, PhD; Michiko Yagoshi, MT; Yumiko Tanimichi, MT; Hiroko Yamada, MT; Kazuo Shimoguchi, MT; Sachiyo Yamamoto, MT; Mitsuru Yanai, MD, PhD; Kazunari Kumasaka, MD, PhD

Disclosures

Am J Clin Pathol

Abstract and Introduction

Abstract

We assessed the usefulness of reporting direct blood Gram stain results compared with the results of positive blood cultures in 482 episodes and monitored impact on selection of antimicrobial treatment. We found that the reporting groups "Staphylococcus spp," "Pseudomonas spp and related organisms," and "yeasts" identified in this way matched perfectly with later culture identification. When the report indicated Staphylococcus spp or Pseudomonas spp and related organisms, physicians started or changed antimicrobials suitable for these bacteria more frequently than when "other streptococci" and "family Enterobacteriaceae" were reported (P < .05). Incorrect recognition of Acinetobacter spp as Enterobacteriaceae family is still the most challenging problem in this context. Gram stain results that definitively identify Staphylococcus spp, Pseudomonas spp and related organisms, and yeasts reliably can be rapidly provided by clinical laboratories; this information has a significant impact on early selection of effective antimicrobials. Further investigation is needed to assess the clinical impact of reporting Gram stain results in bacteremia.

Introduction

Clinically significant bacteremia is an important cause of serious morbidity and mortality. In a previous report of 843 episodes of positive blood cultures from 707 patients, bacteremia-associated mortality was 17.5%.^[1] In another report of 955 bacteremic episodes, mortality due to unidentified organisms was 44%, and even when the organisms were known, mortality was still as high as 25%.^[2]

To reduce mortality and morbidity in bacteremic patients, it is necessary to initiate effective antimicrobial therapy as soon as possible. Many reports indicate a relationship between inadequate antimicrobial therapy and unsatisfactory outcome.^[3–8] Bacteremia frequently causes sepsis and septic shock. Because prompt institution of therapy active against the causative pathogen is one of the most important predictors of outcome, physicians must establish a system for rapid administration of a rationally chosen drug or combination of drugs.^[9]

The clinical microbiology laboratory has an important role in the management of bacteremia. Detecting pathogenic microorganisms in blood cultures and testing antimicrobial susceptibility always assists in selecting the appropriate antimicrobial agent. The most important and primary test to perform on any positive blood culture is Gram stain,^[10] which is the most rapid and simplest test to characterize microorganisms. It is therefore highly likely that the information provided by the Gram stain will help to assess the adequacy of antimicrobial therapy selected after collecting blood culture specimens and before final identification of the microorganism.^[11] In recent reports, the impact of Gram stain results on patient mortality has been documented.^[12–15] On the other hand, there remains the possibility that Gram stain results do not match with the final identification of microorganisms. This would carry a risk leading to inadequate antimicrobial therapy and potentially affecting patients' clinical course and mortality.

The aim of our study was to assess the advantages and disadvantages of reporting Gram stain results for selecting antimicrobial agents and correlating these results with the patients' hospital courses.

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Table 1. Clinical Data for 482 Episodes of Positive Blood Cultures*
Variable	Result
Median age (range), y	67 (0–96)
M/F	291/191
Department
Gastroenterology and hepatology	78 (16.2)
Hematology and rheumatology	70 (14.5)
Emergency and critical care medicine	59 (12.2)
Digestive surgery	55 (11.4)
Cardiovascular surgery	31 (6.4)
Other	189 (39.2)
Site of infection
Bloodstream, catheter-related	173 (35.9)
Undetermined	91 (18.9)
Gastrointestinal/biliary tract	68 (14.1)
Urinary tract	53 (11.0)
Respiratory tract	41 (8.5)
Skin/soft tissue	23 (4.8)
Other	33 (6.8)
Predisposing condition
Malignant disease	210 (43.6)
Chemotherapy	104 (21.6)
Immunosuppressive therapy	88 (18.3)
Diabetes mellitus	76 (15.8)
WBC count < 1,000/μL (1.0 × 10⁹/L)	55 (11.4)
Liver cirrhosis	39 (8.1)
Hemodialysis or peritoneal dialysis	35 (7.3)
Radiation therapy	31 (6.4)

* Data are given as number (percentage) unless otherwise indicated.

Table 2. Changes in Antimicrobial Therapy After Results of Gram Stain Reported*
Suspected Microorganism Based on Gram Stain	No. (%) of Episodes	Start Abx	Adjust Spectrum	Add Other Abx	Other	Total	No Change	Patient Already Died	Other	Total
Gram-positive cocci
Staphylococcus spp	178 (36.9)	20 (11.2)	21 (11.8)	34 (19.1)	32 (18.0)	107 (60.1)†	67 (37.6)	1 (0.6)	3 (1.7)	71 (39.9)
Streptococcus
Streptococcus pneumoniae	12 (2.5)	0 (0)	0 (0)	0 (0)	4 (33)	4 (33)	6 (50)	2 (17)	0 (0)	8 (67)
Other streptococci	35 (7.3)	0 (0)	1 (3)	8 (23)	6 (17)	15 (43)†	20 (57)	0 (0)	0 (0)	20 (57)
Other gram-positive cocci/undetermined	3 (0.6)	0 (0)	0 (0)	2 (67)	0 (0)	2 (67)	1 (33)	0 (0)	0 (0)	1 (33)
Gram-positive rods
Corynebacterium spp	4 (0.8)	0 (0)	1 (25)	2 (50)	0 (0)	3 (75)	0 (0)	0 (0)	1 (25.0)	1 (25)
Gram-negative cocci
Neisseria/Moraxella spp	1 (0.21)	0 (0)	0 (0)	0 (0)	1 (100)	1 (100)	0 (0)	0 (0)	0 (0)	0 (0)
Gram-negative rods
Enterobacteriaceae family	147 (30.5)	10 (6.8)	0 (0.0)	5 (3.4)	30 (20.4)	45 (30.6)†	98 (66.7)	4 (2.7)	0 (0.0)	102 (69.4)
Pseudomonas spp and related organisms	27 (5.6)	0 (0)	0 (0)	3 (11)	13 (48)	16 (59)†	11 (41)	0 (0)	0 (0)	11 (41)
Other gram-negative rods/undetermined	16 (3.3)	0 (0)	0 (0)	0 (0)	4 (25)	4 (25)	11 (69)	1 (6)	0 (0)	12 (75.1)
Fungi
Yeasts	21 (4.4)	0 (0)	1 (5)	8 (38)	3 (14)	12 (57)	7 (33)	2 (10)	0 (0)	9 (43)
Multiple microorganisms	38 (7.9)	3 (8)	1 (3)	5 (13)	9 (24)	18 (47)	20 (53)	0 (0)	0 (0)	20 (53)
Total	482 (100.0)	33 (6.8)	25 (5.2)	67 (13.9)	102 (21.2)	227 (47.1)	241 (50.0)	10 (2.1)	4 (0.8)	255 (52.9)

Abx, antimicrobials.
* Data are given as number (percentage). "Adjust spectrum" means that antimicrobials selected for empiric therapy did not cover microorganisms detected by Gram stain; more effective antimicrobials were then substituted.
† P < .05.

Table 3. Suspected Microorganisms and Accuracy of Gram Stain*
Suspected Microorganism by Gram Stain	Total Episodes	Gram Stain Results Matched Culture Identification	Mismatched Episodes
Gram-positive cocci
Staphylococcus spp	178 (36.9)	178 (100.0)	0 (0.0)
Streptococcus
Streptococcus pneumoniae	12 (2.5)	12 (100)	0 (0)
Other streptococci	35 (7.3)	35 (100)	0 (0)
Other gram-positive cocci/undetermined	3 (0.6)	2 (67)	1 (33.3)
Gram-positive rods
Corynebacterium spp	4 (0.8)	4 (100)	0 (0)
Gram-negative cocci
Neisseria/Moraxella spp	1 (0.2)	1 (100)	0 (0)
Gram-negative rods
Enterobacteriaceae family	147 (30.5)	138 (93.9)	9 (6.1)
Pseudomonas spp and related organisms	27 (5.6)	27 (100)	0 (0)
Other gram-negative rods/undetermined	16 (3.3)	16 (100)	0 (0)
Fungi
Yeasts	21 (4.4)	21 (100)	0 (0)
Multiple microorganisms	38 (7.9)	36 (95)	2 (5)
Total	482 (100.0)	470 (97.5)	12 (2.5)

* Data are given as number (percentage).

Table 4. Details for Episodes With Incorrect Identification by Gram Stain and Progress of Antimicrobial Therapy
Gram Stain/Reported Result/Episode No.	Culture Result	Antimicrobial Therapy		Antimicrobial Agent
Gram Stain/Reported Result/Episode No.	Culture Result	After Stain Result Reported	After Identification and Susceptibility Reported	After Stain Result Reported	After Identification and Susceptibility Reported
GPC/undetermined gram-positive cocci
1	Acinetobacter baumannii	No change	Change by resistance	ZOX	CIP
GNR/Enterobacteriaceae family
2	A baumannii	No change	Narrow spectrum	CAZ and ABK	CAZ and GEN
3	Acinetobacter lwoffi	Change from SAM	Reduce No. of antimicrobials	CAZ and GEN	CAZ
4	A lwoffi	No change	Change by resistance	CIP	PAPM/BP
5	A baumannii	No change	Adjust spectrum	CMZ	CAZ
6	A baumannii	No change	No change	PAPM/BP and AMK	PAPM/BP and AMK
7	A baumannii	No change	No change	PAPM/BP	PAPM/BP
8	Pseudomonas aeruginosa	No change	No change	MPM and AMK	MPM and AMK
9	P aeruginosa and Enterobacter cloacae	No change	Adjust spectrum	CTX	CAZ
10	P aeruginosa and Stenotrophomonas maltophilia	No change	Adjust spectrum	CTX	CAZ
Multiple (GPC + GNR)/Staphylococcus spp + Enterobacteriaceae family
11	P aeruginosa	No change	Adjust spectrum	CMZ	CAZ
Multiple (GNR + GPR)/Pseudomonas spp and related organisms + Bacillus spp
12	P aeruginosa and Clostridium perfringens	Change from CTX	Add other antimicrobials	CAZ and TOB	CAZ, TOB, PEN, and CLI

ABK, arbekacin; AMK, amikacin; CAZ, ceftazidime; CIP, ciprofloxacin; CLI, clindamycin; CMZ, cefmetazole; CTX, cefotaxime; GEN, gentamicin; GNR, gram-negative rods; GPC, gram-positive cocci; GPR, gram-positive rods; MPM, meropenem; PAPM/BP, panipenem/betamiprone; PEN, penicillin G; SAM, ampicillin/sulbactam; TOB, tobramycin; ZOX, ceftriaxone.

Table 5. Clinical Information for 12 Patients With Incorrect Gram Stain Results
Case No./Sex/Age (y)	Culture Result	Site of Infection	Clinical Department	Predisposing Condition	Other Therapy	WBC Count (/μL)*	Outcome	Hospital Days
1/F/77	Acinetobacter baumannii	Undetermined	Psychiatry	Depression	—	11,700	Alive	23
2/F/58	A baumannii	Pharynx	Hematology and Rheumatology	Adult T-cell leukemia	Cx, Im	3,600	Alive	66
3/M/79	Acinetobacter lwoffi	Undetermined	Gastroenterology and Hepatology	Liver cirrhosis, hepatocellular carcinoma	—	8,100	Died	57
4/M/69	A lwoffi	Pharynx	Otolaryngology	Laryngeal carcinoma	Cx, Rx	4,300	Died	54
5/F/73	A baumannii	Urinary tract	Digestive Surgery	Gastric carcinoma	Cx	1,900	Alive	144
6/M/10	A baumannii	Undetermined	Pediatrics	Acute lymphocytic leukemia	Cx, Im	5,200	Alive	418
7/F/74	A baumannii	Intravenous catheter	Otolaryngology	Mandibular carcinoma	Cx	2,000	Died	88
8/M/49	Pseudomonas aeruginosa	Undetermined	Hematology and Rheumatology	Burkitt lymphoma	Cx, Im	100	Died	240
9/M/53	P aeruginosa and Enterobacter cloacae	Undetermined	Otolaryngology	Laryngeal carcinoma	Cx, Rx	7,900	Alive	120
10/M/75	P aeruginosa and Steno-trophomonas maltophilia	Undetermined	Gastroenterology and Hepatology	Alcoholic liver cirrhosis	—	10,200	Died	99
11/M/48	P aeruginosa	Biliary tract	Diabetes and Metabolism	Biliary tract stone	—	11,600	Alive	32
12/F/76	P aeruginosa and Clostridium perfringens	Lower intestine	Gastroenterology and Hepatology	Liver cirrhosis, hepatocellular carcinoma	—	8,900	Died	34

Cx, chemotherapy; Im, immunosuppressive therapy; Rx, radiation therapy.
* Values are given in conventional units; to convert to Système International units (× 109/L), multiply by 0.001.

Table 6. Outcome of Episodes of Major Misrecognized Species by Gram Stain
Cultured Microorganism	No. of Episodes	Gram Stain Results
		Incorrect		Correct
		No. (%) of Deaths	Median Hospital Days (Range)	No. (%) of Deaths	Median Hospital Days (Range)
Gram-negative rods
Acinetobacter spp	8	2/7 (29)	77 (54–418)	1/1 (100)	31
Pseudomonas spp	27	2/3 (67)	99 (56–240)	10/24 (42)	69 (0–376)
Multiple microorganisms	40	2/4 (50)	32 (23–99)	11/36 (31)	55 (0–216)

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Impact of Reporting Gram Stain Results from Blood Culture Bottles on the Selection of Antimicrobial Agents

Abstract and Introduction

Abstract

Introduction

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Authors and Disclosures

Authors and Disclosures

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