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133（ 61 ）Investigation of the risk factors of anaerobic
bacteremia in a case–control study
TAKUMI UMEMURA1,2, YUKA YAMAGISHI1,3, YUKIHIRO HAMADA3,HIROYUKI SUEMATSU3 and HIROSHIGE MIKAMO1,3
1

Department of Clinical Infectious Deseases, Aichi Medical University
Graduate School of Medicine
2
Department of Pharmacy, Tosei General Hospital3
Department of Infection Control and Prevention,
Aichi Medical University Hospital(Received for publication February 14, 2014)

Background: Many case series studies have reported risk factors of infection
with anaerobic bacteria, but few factor analysis studies have been conducted.
Objective: We conducted a case–control study to identify the risk factors ofanaerobic bacteremia.
Methods: We compared a number of characteristics of patients with anaerobic
bacteremia with those with aerobic bacteremia. Clinical information for 71 patientsof anaerobic bacteremia was collected from January 1999 to December 2012 in$LFKL0HGLFDO8QLYHUVLW\+RVSLWDO)RUHDFKFDVHZHLGHQWL¿HGXSWRIRXUFRQWUROV
matched by the time of the positive blood culture.
Results: Multivariate logistic analyses revealed an association between
anaerobic bacteremia and malignancy (OR: 3.35, 95%CI: 1.85–6.09), Douglasʼ
pouch drains (OR: 25.90, 95%CI: 2.90–25.00) and chest drains (OR: 3.35, 95%CI:
1.19–9.43) as the primary causative disease, as well as associations between
anaerobic bacteremia and the gastrointestinal tract (OR: 3.29, 95%CI: 1.38–7.81) ,genitourinary tract (OR: 4.98, 95%CI: 2.06–12.05), Douglasʼ pouch drains (OR:
16.95, 95%CI: 1.82–166.67) and chest drains (OR: 3.62, 95%CI: 1.29–10.20) as theprimary causative organs. On the other hand, our study showed that having a central
venous catheter was not associated with anaerobic bacteremia.
Conclusions: We demonstrated an association between anaerobic bacteremia
and malignancy, gastrointestinal and genitourinary tracts, patients having a Douglasʼ
SRXFK GUDLQV RU FKHVW GUDLQV 7KHVH ¿QGLQJV PD\ EH XVHIXO IRU GHYHORSLQJ HDUO\appropriate management for anaerobic bacteremia.

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Introduction
It is widely accepted that the presence of anaerobes in the blood stream is associated withmortality. The detection rate of anaerobes in blood cultures is 1–17%, depending on the institution1〜6). Some studies report a decrease in the number of blood cultures testing positive for anaerobes6〜9). The presence of Bacteroides in the blood of patients with bacteremia is increasing9),
and a greater proportion of patients with anaerobic bacteremia present with underlying malignancies, diabetes, and gastrointestinal surgery2,10,11).
In addition, anaerobic bacteremia has been associated with a poor clinical outcome, necessitating appropriate therapy12,13). It remains uncertain whether the rates of anaerobic bacterial infection are increasing or decreasing, and the accurate detection of anaerobes depends on the clinicalODERUDWRU\RIVSHFL¿FLQVWLWXWLRQV%HFDXVHRIWKHVHIDFWRUVLWLVLPSRUWDQWWRUHFRJQL]HWKHULVN
factors of anaerobic bacteremia in order to take quick and appropriate action. Many case series
studies have reported risk factors of infection with anaerobic bacteria5,14,15), but few factor analysis studies have been conducted. As such, we initiated a case–control study to identify these risk
factors using a more valid methodology.

Material and Methods
Setting
This study was conducted from January 1999 to December 2012 in Aichi Medical University+RVSLWDO EHGV )RUEORRGFXOWXUH%'UH]XQERWWOHV %HFWRQ'LFNLQVRQ &R7RN\R-DSDQ 
ZHUH XVHGDQG WKH %' %$&7(& );EORRGFXOWXUHV\VWHP %HFWRQ'LFNLQVRQ &R7RN\R
Japan) was employed for the growth and detection of anaerobes. Each pair of aerobic and anaeroELFERWWOHVZDVLQFXEDWHGIRURQHZHHNLQWKLVV\VWHP$OOSDWLHQWLGHQWL¿HVZHUHUHPRYHGEHIRUH
analysis. This study was approved by the ethical committee of Aichi Medical University Hospital.
Case–control study'H¿QLWLRQRIFDVHVDQGFRQWUROV
Patients with blood cultures positive for anaerobic bacteria included as cases and were retroVSHFWLYHO\LGHQWL¿HGXVLQJIMZLQJEDFWHULDOWHVWV\VWHPV )XML7HFKQR6XSSO\&R %DFWHUHPLD ZDV GHHPHG FOLQLFDOO\ VLJQL¿FDQW ZKHQ WKH SDWLHQW KDG RQH RU PRUH SRVLWLYH
blood cultures and met one of the following criteria: white blood cell count ＜4000 or＞12,000/ȝL; temperature ＞38°C; or physical, pathological, or surgical evidence consistent with
infection (e.g., isolation of anaerobic bacteria from a source other than blood)16). Patients with
PropionibacteriumVSHFLHVIURPEORRGFXOWXUHZHUHGH¿QHGDVFOLQLFDOO\VLJQL¿FDQWXVLQJSUHYLously cited criteria16,17).

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135（ 63 ）)RUHDFKFDVHZHLGHQWL¿HGXSWRIRXUFRQWUROVPDWFKHGE\WKHWLPHRIWKHSRVLWLYHEORRG
culture (within one week)18〜20)&OLQLFDOVLJQL¿FDQFHZDVGHWHUPLQHGXVLQJWKHVDPHFULWHULDDV
OLVWHGDERYHDQGFRQWUROVZLWKFOLQLFDOO\LQVLJQL¿FDQWEDFWHUHPLDZHUHH[FOXGHG
Variables:HUHFRUGHGWKHVH[DJH>FKLOGUHQ 侑15 years) and the elderly (侒65 years)], body temperature (°C), over 48 hours after admission, abscess formation, necrosis, ICU admission history,
steroid use within four weeks, anticancer agent use within four weeks, blood glucose level(侒140 mg/dL)21) SULPDU\ FDXVDWLYH GLVHDVH DQG SULPDU\ FDXVDWLYH RUJDQ FODVVL¿HG DFFRUGLQJ WR
,QWHUQDWLRQDO 6WDWLVWLFDO &ODVVL¿FDWLRQ RI 'LVHDVHV DQG 5HODWHG +HDOWK 3UREOHPV th Revision(ICD-10)22), and type of catheter or drain used.
Statistical analysis
4XDOLWDWLYH DQG VWUDWL¿HG FRQWLQXRXV YDULDEOHV ZHUH FRPSDUHG XVLQJ )LVKHUʼV H[DFW WHVW RU
Pearsonʼs Ȥ2 test. Continuous variables were compared using Studentʼs t-test or the Mann-Whitney U test as appropriate. Multivariate logistic analyses were used for logistic regression models.
The variables that achieved a p value ＜0.1 in univariate logistic analyses were included in themultivariate analysis23). Predictive values are presented as odds ratios (ORs) with their 95% con¿GHQFHLQWHUYDOV &, p values ＜ZHUHFRQVLGHUHGVWDWLVWLFDOO\VLJQL¿FDQW:HVHSDUDWHGSULmary disease groups and primary disease organs for multivariate logistic analyses to avoid duplicate risk factors. Analyses were performed using IBM SPSS Statistics 19 (IBM®).

Results
Table 1 shows blood culture yield at Aichi Medical University Hospital. In one year, 601–
Table 1. Blood culture yield at Aichi Medical University Hospital136（ 64 ）THE JAPANESE JOURNAL OF ANTIBIOTICS

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3666 sets of aerobic and anaerobic blood cultures were performed. For each year, 14.8–24.0%
samples tested positive for aerobic and anaerobic bacteria, and positive tests for anaerobes were0.26–0.92% that increasing tendency.
Seventy-one anaerobic bacteremia and 262 aerobic bacteremia patients were eligible for thisstudy. Table 2 shows the data for all anaerobic bacteria isolated from blood culture in bacteremia
patients. The most common anaerobic organisms were Bacteroides sp., followed by Clostridium
sp. and Prevotella sp. ,Q WKLV VWXG\ DSSUR[LPDWHO\ KDOI RI WKH DQDHUREHV ZHUH XQLGHQWL¿HG EHFDXVHDQDHURELFEDFWHULDLGHQWL¿FDWLRQZDVQRWURXWLQHO\FRQGXFWHG
Univariate logistic analysis
Table 3 shows the baseline characteristics and univariate logistic regression analyses of patient histories. Each variable was evaluated using univariate logistic analysis. Variables with pvalue ＜ZHUH>PDOLJQDQF\@>LQMXU\@>GLVHDVHVRIWKHPXVFOH@>SHULWRQHXP@>FLUFXODWRU\V\VWHP@>JDVWURLQWHVWLQDOWUDFW@>JHQLWRXULQDU\WUDFW@>'RXJODVʼSRXFKGUDLQV@DQG>FKHVWGUDLQV@
Multivariate logistic analysis
The variables with p value ＜ZHUHH[DPLQHGXVLQJPXOWLYDULDWHORJLVWLFDQDO\VLV7KHUH
ZHUH IHZ DQDHURELF EDFWHUHPLD SDWLHQWV ZLWK WKH FODVVL¿FDWLRQ RI >LQMXU\@ DQG >GLVHDVHV RI WKHPXVFOH@DVWKHSULPDU\FDXVDWLYHGLVHDVHRUWKH>FLUFXODWRU\V\VWHP@DQG>SHULWRQHXP@DVWKHSULPDU\FDXVDWLYHRUJDQZHUHWKXVH[FOXGHGIURPPXOWLYDULDWHORJLVWLFDQDO\VHV
0XOWLYDULDWH ORJLVWLF UHJUHVVLRQ DQDO\VLV RI SULPDU\ FDXVDWLYH GLVHDVH DQG WKH W\SH RI
catheter or drain used
Table 4 shows the results of multivariate logistic regression analysis of the primary causative
disease and the type of catheter or drain used. Independent risk factors of anaerobic bacteremia
ZHUH>PDOLJQDQF\@ 25&,± >'RXJODVʼ pouch drains] (OR: 25.90, 95%CI:

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7DEOH  8QLYDULDWHORJLVWLFUHJUHVVLRQDQDO\VHVRISDWLHQWVKLVWRULHV

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Table 3. (continued)

7DEOH  0XOWLYDULDWH ORJLVWLF UHJUHVVLRQ DQDO\VLV RI SULPDU\ FDXVDWLYH GLVHDVHV DQG W\SHV RI
catheters and drains

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139（ 67 ）7DEOH  0XOWLYDULDWH ORJLVWLF UHJUHVVLRQ DQDO\VLV RI SULPDU\ FDXVDWLYH RUJDQV DQG W\SHV RI
catheters and drains± DQG>FKHVWGUDLQV@ 25&,± 
0XOWLYDULDWH ORJLVWLF UHJUHVVLRQ DQDO\VLV RI SULPDU\ FDXVDWLYH RUJDQ DQG WKH W\SH RI
catheter or drain used
Table 5 shows the results of multivariate logistic regression analysis of the primary causative
organ and the type of catheter or drain used. Independent risk factors of anaerobic bacteremia
ZHUH >JDVWURLQWHVWLQDO WUDFW@ 25  &, ±  >JHQLWRXULQDU\ WUDFW@ 25 
&, ±  >'RXJODVʼ SRXFK GUDLQV@ 25  &, ±  DQG >FKHVW
drains] (OR: 3.62, 95%CI: 1.29–10.20).

Discussion
In cases where anaerobic bacteremia is suspected, a quick and appropriate action is important . However, few factor analysis studies have been reported, and no previous studies havecompared patients with anaerobic bacteremia with those with aerobic bacteremia. This case–control study was conducted to identify the risk factors of anaerobic bacteremia using aerobic
bacteremia patients as controls.
5HVXOWV RI WKH FXUUHQW VWXG\ LQGLFDWHG WKDW DJH >FKLOGUHQ 侑15 years) and the elderly (侒65
years)] was not associated with anaerobic bacteremia. SAITO reported that the mean age of patients
ZLWKFOLQLFDOO\VLJQL¿FDQWDQDHURELFEDFWHUHPLDZDV\HDUVLQIRXUXQLYHUVLWLHVDQGRQHFRPmunity hospital case series study24); similarly, the mean age in the current study was 63.9 years.
In addition, OGURI reported in a 41-year case series study that 50% patients with anaerobic bacteremia were over 60 years25), and FINEGOLD et al. reported that the elderly were at a higher risk ofanaerobic bacteremia than infants26)+RZHYHURXU¿QGLQJVUHYHDOHGWKDWDJHZDVQRWDFKDUDFWHUistic risk factor of anaerobic bacteremia because there was little difference between case and control patients (Table 3). High blood glucose levels is a risk factor of various types of infection10,22,27), but our study showed it was not a unique risk factor of anaerobic bacteremia (Table 3).
13)140（ 68 ）THE JAPANESE JOURNAL OF ANTIBIOTICS

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In this study, multivariate logistic regression analysis of the primary causative disease andthe type of catheter or drain revealed that malignancy increased the risk of anaerobic bacteremia
7DEOH 7KLVREVHUYDWLRQLVFRQVLVWHQWZLWKWKDWRISUHYLRXVUHSRUWV)RUH[DPSOH6AITO et al.
reported that 49% patients with anaerobic bacteremia had malignancy24). Similarly, OGURI et al.
reported that 77.2% anaerobic bacteremia patients had some type of malignancy25), and multiple
institutional and long-term case series studies reported that numerous patients with anaerobic
bacteremia had malignancy as the primary causative disease13,28)2XU¿QGLQJVLQGLFDWHGWKDWSDWLHQWVZLWKPDOLJQDQF\KDGDVSHFL¿FULVNUDWLR 25 RIIRUDQDHURELFEDFWHUHPLDFRPSDUHG
with patients with aerobic bacteremia. This result has some unknown reasons. It has been suggested that these are causal factors, and it is important to consider the presence of anaerobes inpatients with malignancies who are suspected of having bacteremia.
In a multivariate logistic regression analysis of the primary causative organ and type of catheter or drain used, gastrointestinal tract as the primary causative organ increased the risk (OR: RIDQDHURELFEDFWHUHPLD 7DEOH $QDHURELFEDFWHULDDUHLQGLJHQRXVÀRUDRIWKHLQWHVWLQDO
tract29), primarily consisting of Clostridium and B. fragilis30), which is consistent with previous
studies. ROBERT et al.16) and OGURI et al.25) reported that in 52% and 46.5% patients, respectively,
anaerobic bacteremia originated from the digestive tract. BROOK et al. subsequently reported thatthe primary portal of entry for bacteria was the gastrointestinal tract28). FRAINSTEIN et al. reported
that one of the most common malignancies was gastrointestinal malignancy31). The results of ourVWXG\FRUURERUDWHWKHVH¿QGLQJV
In addition, in a multivariate logistic regression analysis of the primary causative organ andtype of catheter or drain used, disease of the genitourinary tract increased the risk (OR: 4.98) of
anaerobic bacteremia (Table 5). Some studies have reported an increase in anaerobic bacteremia
among patients with genitourinary malignancies. Bacteroides and Clostridium are often detectedin anaerobic bacterial infections of the genitourinary tract, and these can cause severe infections30).
In general, anaerobic genitourinary tract infection frequently occurs in females. In our study, nineof the 12 case patients were female (data was not shown), but only four females had genitouriQDU\WUDFWLQIHFWLRQZKLOHWKHRWKHUVKDGPDOLJQDQFLHV,QRUGHUWRFRQ¿UPWKLV¿QGLQJDGGLWLRQDO
long-term studies at multiple institutions are necessary.
In a multivariate logistic regression analysis, Douglasʼ pouch drains and the chest drains increased risk of anaerobic bacteremia (Tables 4 and 5). Douglasʼ pouch and the chest are sites
where anaerobic bacteria are often detected by cultivation tests30,32). Drainage is performed whenabscesses are present in these locations, and we suggest that abscess formation increases the riskof anaerobic bacteremia.
On the other hand, our study showed that having a central venous (CV) catheter was not asVRFLDWHG ZLWK DQDHURELF EDFWHUHPLD 7DEOH   EXW WKLV ¿QGLQJ ZDV QRW VWDWLVWLFDOO\ VLJQL¿FDQW+RZHYHUWKLV¿QGLQJPD\KDYHEHHQWKHUHVXOWRIQRWLQFOXGLQJDQ\SDWLHQWVZLWKPropionibacte-Apr. 2014

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141（ 69 ）rium infection, which is an indigenous bacterium of the skin, because coagulase-negative staphylococci (such as Staphylococcus epidermidis) frequently cause bacteremia when a CV catheter ispresent.
However, our study had some limitations. First, our results were based on a retrospective review of routine microbiology data. We may have missed additional risk factors since our data inFOXGHV D VPDOO VDPSOH VL]H 6HFRQG RXU VWXG\ LV  \HDUV ORQJ WHUP VWXG\ EXW RQH LQVWLWXWLRQ
study, so patients of anaerobic bacteremia are not enough. Additional long-term prospective studies at multiple institutions are required to investigate a larger number of patients and to identify
those risk factors using multivariate logistic analyses.
In conclusion, by using multivariate logistic analysis, we demonstrated an association between anaerobic bacteremia and malignancy as the primary causative disease, as well as associations between anaerobic bacteremia and the gastrointestinal and genitourinary tracts as the primary causative organs. In addition, the study revealed associations between anaerobic bacteremia
and having a Douglasʼ pouch drains or chest drains. The results of this study are important forearly and appropriate management of anaerobic bacteremia.
$FNQRZOHGJPHQWV
We thank all clinicians and pharmacists that have assisted with the provision of data for thisSURMHFW&RQÀLFWRILQWHUHVW
7KHDXWKRUVVWDWHWKDWWKH\KDYHQRFRQÀLFWRILQWHUHVWZLWKWKHVXEMHFWPDWWHUGLVFXVVHGLQ
this article.

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