Are We “Squeezing The Balloon” When Reducing the Risk of Occupational Infection?

Reply to
Pan et al. •
Author(s): Ignacio Galed Placed , MD
Source: Infection Control and Hospital Epidemiology, Vol. 29, No. 1 (January 2008), pp. 95-96
Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiology
of America
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 infection control and hospital epidemiology
letters to the editor
Surgical Site Infections After
Laparoscopic and Open Cholecystectomies
in Community Hospitals
t o t h e e d i t o r — Laparoscopic cholecystectomy has be-
come the preferred method of performing gallbladder surgery
over the past decade. Laparoscopic cholecystectomies are as-
sociated with shorter hospital stay and convalescence, less
pain and scarring, and lower rates of postoperative surgical
site infection (SSI) than open cholecystectomies.1-4 The fact
that laparoscopic cholecystectomies are associated with fewer
SSIs intuitively makes sense: laparoscopy access ports are
short in length and only a fraction of the length of the incision
used in open laparotomy. Biscione et al.5 reported in the
September issue of the journal that patients who underwent
laparoscopic cholecystectomy had lower rates of incisional
SSI than patients who underwent open cholecystectomy;
however, rates of deep incisional/organ space infections were
similar in these 2 groups.5 The latter finding differs from our
experience and from the results reported in the existing lit-
erature, for several reasons.
Although 80% of all cholecystectomies in the United States
were performed laparoscopically in 2002,6 only 59% of cho-
lecystectomies were performed laparoscopically in the Bis-
cione et al. study.5 Furthermore, their results showed that the
use of laparoscopic cholecystectomy decreased over time,
declining from 62% of procedures in 1996-1999 to 57% in
2000 and later. The authors offered no explanation for this
decline. We suspect that the criteria for choosing open or
laparoscopic cholecystectomy for the patients selected for this
study were different from the criteria used in current practice
in the United States. However, it is also possible that the
higher proportion of open procedures performed in the study
by Biscione et al.5 was the result of high rate of conversion
from laparoscopic to open procedures as a result of technical
difficulties.
The study by Biscione et al.5 was probably underpowered
to assess whether the rate of deep SSI was the same or different
in patients undergoing open procedures and patients under-
going laparoscopic procedures. The authors examined 5,848
procedures and observed a total of 39 deep incisional or organ
space infections. In contrast, a study that showed a reduced
rate of deep incisional or organ space infection following
laparoscopic surgery examined 10 times that number of pro-
cedures (54,504) and observed almost 7 times as many deep
incisional/organ space infections (294).7
Finally, the high overall SSI rate in the study by Biscione
et al.5 restricted the generalizability of their findings. Biscione
et al.5 reported 3.57 infections per 100 procedures, whereas
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january 2008, vol. 29, no. 1
the 2004 National Nosocomial Infection Surveillance (NNIS)
system data showed 3.23 infections per 100 cholecystectomies
in US hospitals for patients with the highest NNIS risk index
score.8 We commend Biscione et al.5 for providing valuable
data on cholecystectomies in community hospitals. However,
the results from the study do not appear to reflect the practice
in most US hospitals.
We analyzed data collected by the Duke Infection Control
Outreach Network on the rate of SSI following cholecystec-
tomy to determine whether our findings were the same or
dissimilar to those reported by Biscione et al.5 Data on the
risk of SSI were prospectively collected from 38,232 patients
who underwent cholecystectomy in 31 community hospitals
in the southeastern United States during the period from 1991
to 2007. The median size of the participating hospitals was
220 beds (range, 39-537 beds). We determined the rates of
SSI for laparoscopic and open cholecystectomies and then
stratified the rates by age, NNIS risk index score, American
Society of Anesthesiologists classification, wound class, and
the year that surgery was performed. Hypothesis testing was
performed with the x2 test for categorical variables, 2-tailed
P values, and an a of .05.
A total of 145 SSIs were identified following 38,232 cho-
lecystectomies (ie, 0.38 infections per 100 procedures) during
the 15-year study period (Table); 35,316 (94%) of these cho-
lecystectomies were performed laparoscopically. The median
patient age was 49 years. Open cholecystectomy was per-
formed more often for older patients: the proportion of
patients older than 60 years of age was 47% in the open
cholecystectomy group and 29% in the laparoscopic chole-
cystectomy group (P ! .001). Open cholecystectomy was per-
formed more often during the 1990s than it was after 2000:
from 1991 to 2000, a total of 75% of cholecystectomies were
performed laparoscopically; 94% of all procedures were done
laparoscopically after 2000 (P ! .001).
The SSI rate was 1.37 infections per 100 open cholecys-
tectomies and 0.30 infections per 100 laparoscopic procedures
(relative rate ratio, 4.61 [95% confidence interval, 4.29-4.97];
P ! .001). We also performed subgroup analyses after strat-
ifying the data by NNIS risk index score, age (older than 60
years), American Society of Anesthesiologists classification,
wound class, surgical duration (more than 120 minutes or
120 minutes or less), and the year in which the operation
was performed (before or after 2000). Laparoscopic chole-
cystectomies consistently had lower rates of SSI, compared
with open procedures in all subgroups; with significant P
values for each analysis, except for one comparison (Table).
The type of surgery (laparoscopic or open) remained signif-
icantly associated with SSI in a multivariable model that con-
trolled for all significant variables in the univariate analysis.
For the reasons cited above, we think that it is unwise to
generalize the findings reported by Biscione et al.5 to patients
 letters to the editor 93

table Rates and Relative Rate Ratios for Surgical Site Infection (SSI) Following Open and Laparoscopic
Cholecystectomies in a Cohort of 38,232 Patients from 31 Community Hospitals
Open procedure Laparoscopic procedure
(n p 2,916) (n p 35,316)
Relative rate ratio
Variable SSIs/proceduresa SSI rateb SSIs/proceduresa SSI rateb (95% CI) P
Overall 40/2,916 1.37 105/35,316 0.30 4.61 (3.21– 6.62) !.001
Patient characteristic
NNIS risk index score
0 6/1,067 0.56 44/22,926 0.19 2.93 (1.25-6.86) !.001
1 15/1,357 1.11 49/11,087 0.44 2.50 (1.41-4.45) !.001
x2 19/492 3.86 12/1,303 0.92 4.19 (2.05-8.57) !.001
Age
X60 years 12/1,551 0.77 54/25,052 0.22 3.59 (1.92-6.70) !.001
160 years 28/1,365 2.05 51/10,264 0.50 4.12 (2.61-6.52) !.001
ASA classification
!3 14/1,585 0.88 52/24,820 0.21 4.21 (2.34-7.59) !.001
x3 25/1,331 1.95 53/10,496 0.50 3.87 (2.42-6.16) !.001
Surgical duration
X120 minutes 20/2,069 0.97 91/33,107 0.27 3.52 (2.17-5.69) !.001
1120 minutes 20/847 2.36 14/2,209 0.63 3.73 (1.89-7.34) !.001
Wound class
CL-CC 32/2,762 1.16 100/34,444 0.29 3.99 (2.69-5.93) !.001
CO-I 8/154 5.19 5/872 0.57 9.06 (3-27.3) !.001
Time of surgery
Before 2000 6/894 0.67 10/2,648 0.38 1.78 (0.65-4.88) .26
After 2000 34/2,022 1.68 95/32,668 0.29 5.78 (3.92-8.53) !.001

note. ASA, American Society of Anesthesiologists physical status; CC, clean contaminated; CL, clean; CO, contam-
inated; I, infected; NNIS, National Nosocomial Infection Surveillance system.
a
No. of SSIs / no. of procedures.
b
No. of infections per 100 procedures.

in the United States. In fact, it may not be possible to use
data on the risk of SSI following cholecystectomy that were
collected prior to 2000 to assess the risk of SSI for patients
undergoing this procedure now. Finally, because in modern
practice the majority of open cholecystectomies have been
converted from attempted laproscopic procedures immedi-
ately after they are determined to have been unsuccessful, the
risk of complications following open cholecystectomy is
likely to be quite different than was observed in the recent
past (eg, prior to 2000). However, our review of the risk of
SSI in a cohort of 38,232 patients who underwent chole-
cystectomy supports the findings of other investigators who
have concluded that laparoscopic cholecystectomy is associ-
ated with significantly lower rate of SSI, compared with open
procedures.3,7,9,10
Luke F. Chen, MBBS (Hons), FRACP;
Deverick J. Anderson, MD, MPH;
Matthew G. Hartwig, MD;
Keith S. Kaye, MD, MPH;
Daniel J. Sexton, MD
From the Division of Infectious Diseases, Duke Infection Control Outreach
Network (L.F.C., D.J.A., K.S.K., D.J.S.), and the Department of Surgery
(M.G.H.), Duke University Medical Center, Durham, North Carolina.
Address reprint requests to Luke F. Chen, MBBS, FRACP, 2100 Erwin
Road, Durham, NC, 27710 (luke.chen@duke.edu).
Infect Control Hosp Epidemiol 2008; 29:92-94
䉷 2007 by The Society for Healthcare Epidemiology of America. All rights
reserved. 0899-823X/2008/2901-0019$15.00.DOI: 10.1086/524335
re f e re n c e s
1. Legorreta AP, Silber JH, Costantino GN, Kobylinski RW, Zatz SL. In-
creased cholecystectomy rate after the introduction of laparoscopic cho-
lecystectomy. JAMA 1993; 270:1429-1432.
2. Hendolin HI, Paakonen ME, Alhava EM, Tarvainen R, Kemppinen T,
Lahtinen P. Laparoscopic or open cholecystectomy: a prospective ran-
domised trial to compare postoperative pain, pulmonary function, and
stress response. Eur J Surg 2000; 166:394-399.
3. Zacks SL, Sandler RS, Rutledge R, Brown RS Jr. A population-based
cohort study comparing laparoscopic cholecystectomy and open cho-
lecystectomy. Am J Gastroenterol 2002; 97:334-340.
4. Inoue H, Itoh K-i, Hori H, et al. The cosmetic benefit of three-port
laparoscopic cholecystectomy and umbilical trocar insertion. Dig Endosc
1994; 6:49-51.
5. Biscione FM, Couto RC, Pedrosa TM, Neto MC. Comparison of the risk
of surgical site infection after laparoscopic cholecystectomy and open
cholecystectomy. Infect Control Hosp Epidemiol 2007; 28:1103-1106.
6. Livingston EH, Rege RV. A nationwide study of conversion from lapa-
roscopic to open cholecystectomy. Am J Surg 2004; 188:205-211.
7. Richards C, Edwards J, Culver D, Emori TG, Tolson J, Gaynes R. Does
using a laparoscopic approach to cholecystectomy decrease the risk of
surgical site infection? Ann Surg 2003; 237:358-362.
8. National Nosocomial Infections Surveillance (NNIS) System Report, data

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All use subject to JSTOR Terms and Conditions
94 infection control and hospital epidemiology january 2008, vol. 29, no. 1
summary from January 1992 through June 2004, issued October 2004.
Am J Infect Control 2004; 32:470-485.
9. Chuang SC, Lee KT, Chang WT, et al. Risk factors for wound infection
after cholecystectomy. J Formos Med Assoc 2004; 103:607-612.
10. Williams LF, Jr., Chapman WC, Bonau RA, McGee EC, Jr., Boyd RW,
Jacobs JK. Comparison of laparoscopic cholecystectomy with open cho-
lecystectomy in a single center. Am J Surg 1993; 165:459-465.
Reply to Chen et al.
t o t h e e d i t o r — We really appreciate the interest of Dr.
Chen and colleagues1 in our recent article.2 Several factors
may explain the lower rate of laparoscopic cholecystectomy
in our institutions. It is not the consequence of higher rates
of conversion to open cholecystectomy, because we kept con-
verted procedures in their original surgical group. First, note
that our institutions adopted the National Nosocomial In-
fection Surveillance (NNIS) system’s definition of operative
procedure, which excludes outpatient (same-day) surgical
procedures.3 Thus, same-day laparoscopic cholecystectomies
were excluded from the analysis, lowering the overall pro-
portion of laparoscopic procedures. Furthermore, our in-
creasing use of same-day laparoscopic cholecystectomy in re-
cent years, similar to increases in the use of this procedure
elsewhere around the world, can account for the apparent
reduction in the proportion of laparoscopic cholecystectomy
observed in our series over time. Second, the use of mini-
incision cholecystectomy as an alternative approach to both
open cholecystectomy and laparoscopic cholecystectomy is
rising in frequency in our country. For surveillance purposes,
we consider classic laparotomic cholecystectomies and mini-
incision cholecystectomies to be open cholecystectomies. So,
inclusion of data on procedures with mini-incision access
would lower the rate of laparoscopic cholecystectomy but
leave the rate of open cholecystectomy unchanged.
Third, recall that our institutions are private and not uni-
versity affiliated, and major differences exist in clinical prac-
tices in comparison to public or university-affiliated hospitals.
Although economic concerns are obviously not unique to the
private sector, the economic pressures exerted by health plans
assume a clear role in private institutions, particularly in a
resource-constrained country such as ours. Economic eval-
uations conducted in developed countries have so far favored
laparoscopic cholecystectomy over open cholecystectomy, but
the cost savings of laparoscopic cholecystectomy may be less
apparent in other types of institutions4 or when compared
with minilaparotomy cholecystectomy.5 Moreover, some ways
in which laparoscopic cholecystectomy has demonstrated
clear superiority over open cholecystectomy, such as shorter
associated sick leave, do not necessarily represent a clear ben-
efit to health plans and, accordingly, do not enter in their
cost-effectiveness equations. More importantly, even with the
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All use subject to JSTOR Terms and Conditions
assumption that laparoscopic cholecystectomy is cost effec-
tive, laparoscopic cholecystectomy savings may not overcome
the increased consumption of healthcare resources resulting
from the well-known rise in the number of cholecystectomies
performed and in hospital use after laparoscopic cholecys-
tectomy is introduced.6-8 It is possible that all of these con-
cerns may have limited the availability of laparoscopy in our
institutions to some extent.
That our study might have been underpowered to detect
a lower risk of organ space infections after laparoscopic cho-
lecystectomy was acknowledged in the Discussion section of
our article.2 Chen et al.1 declined to assess the risk of organ
space infection in their study, so the assertion that our finding
differs from their experience is not supported by their data.
It is misleading to consider the study by Richards et al.9 as
valid evidence of reduced risk of organ space infection fol-
lowing laparoscopic cholecystectomy. The lower crude rate
of organ space infection after laparoscopic cholecystectomy
reported in that study was an unadjusted comparison and,
therefore, was not mentioned as a major finding by the au-
thors.9 In that study, patients who underwent laparoscopic
cholecystectomy were obviously less prone to infection than
patients who underwent open cholecystectomy, because la-
paroscopic cholecystectomies were shorter in duration, and
patients who underwent these procedures were younger and
less likely to have an American Society of Anesthesiologists
classification of 3 or greater, dirty or contaminated wounds,
emergency procedures, or multiple procedures performed
through the same incision.9 Therefore, laparoscopic chole-
cystectomy and open cholecystectomy could not be straight-
forwardly compared without a multivariate analysis, which
was only provided for the overall risk of surgical site infection
(SSI).9 We still believe that, if our extensive cohort of 5,848
patients failed to show a difference in the risk of organ space
infection, a potential difference seems to be clinically irrel-
evant in our setting.
Chen et al.1 should note that more caution in needed when
comparing the SSI rates we reported2 with those of the NNIS
system. The most obvious reason for the higher SSI rate in
our cohort was the higher proportion of open cholecystec-
tomies. Second, the NNIS system emphasizes that, for SSI
rate comparisons to be valid, it must be known whether case
finding included infections detected after discharge and the
postdischarge surveillance method must be the same10; how-
ever, their own reports repeatedly fail to declare whether post-
discharge surveillance was actually used and what proportion
of patients were reached by postdischarge surveillance.11 Chen
et al.1 also did not mention whether postdischarge surveil-
lance was used in their study. Therefore, any comparison
between their SSI rates and ours is irrelevant, and inferences
about the generalizability of our data based on such com-
parisons are hasty and inaccurate. In our study, 55.5% of all
SSIs were detected after discharge, even though a modest
49.5% of patients were reached by postdischarge surveillance.2
In the study by Richards et al.,9 only 28.8% of SSIs were

detected after discharge, suggesting that the proportion of
patients reached by out-of-hospital surveillance in that study,
and in NNIS hospitals as a whole, is even less than that in
our study. What renders our practice incomparable to that
of most hospitals in the United States is, first of all, irrec-
oncilable differences in surveillance methods.
For these reasons, we agree with Chen et al.1 that our results
must not be generalized to patients in the United States, and
to the same extent, the results of US studies must not be
generalized to our patients. It is not clear why they suggest
that a study could be generalized to a population other than
that from which the sample was retrieved.
Chen et al.1 should explain further why it may not be
possible to use data on the risk of SSI collected prior to 2000
in a cohort study with concurrent controls. This concern may
be more relevant for a study using historical controls. In-
creases in conversion rates are mainly driven by changes in
the spectrum of indications for laparoscopic cholecystec-
tomy.12 The inclusion of the year of surgery as explanatory
variable was the only possible means to address this in our
data.
acknowledgments
Financial support. F.M.B. reports receiving grant support N§0151041 from
Capes/CNPq- IEL Nacional-Brasil for the original manuscript.
Potential conflicts of interest. The author reports no conflicts of interest
relevant to this article.
Fernando M. Biscione, MD, MSc
From the Health Sciences Postgraduate Course, Medicine High School,
Minas Gerais Federal University, Belo Horizonte, Minas Gerais, Brazil.
Address reprint requests to Fernando M. Biscione, MD, MSc, 190 Alfredo
Balena av., Suite 7003, Santa Efigênia, Belo Horizonte, Minas Gerais, Brazil,
31.130-100 (fernandobiscione@yahoo.com.ar).
Infect Control Hosp Epidemiol 2008; 29:94-95
䉷 2007 by The Society for Healthcare Epidemiology of America. All rights
reserved. 0899-823X/2008/2901-0020$15.00.DOI: 10.1086/524912
ref e re n c e s
1. Chen LF, Anderson DJ, Hartwig MG, Kaye, KS, Sexton DJ. Surgical site
infections after laparoscopic and open cholecystectomies in community
hospitals. Infect Control Hosp Epidemiol 2008; 29:92-94 (in this issue).
2. Biscione FM, Couto RC, Pedrosa TM, Neto MC. Comparison of the risk
of surgical site infection after laparoscopic cholecystectomy and open
cholecystectomy. Infect Control Hosp Epidemiol 2007; 28:1103-1106.
3. Horan TC, Emori TG. Definitions of key terms used in the NNIS system.
Am J Infect Control 1997; 25:112-116.
4. Teerawattananon Y, Mugford M. Is it worth offering a routine laparos-
copic cholecystectomy in developing countries? A Thailand case study.
Cost Eff Resour Alloc 2005; 3:10.
5. Nilsson E, Ros A, Rahmqvist M, Backman K, Carlsson P. Cholecystec-
tomy: costs and health-related quality of life: a comparison of two tech-
niques. Int J Qual Health Care 2004; 16:473-482.
6. Hobbs MS, Mai Q, Fletcher DR, Ridout SC, Knuiman MW. Impact of
laparoscopic cholecystectomy on hospital utilization. ANZ J Surg 2004;
74:222-228.
This content downloaded from 91.229.248.66 on Thu, 15 May 2014 07:58:02 AM
All use subject to JSTOR Terms and Conditions
letters to the editor 95
7. Legorreta AP, Silber JH, Costantino GN, Kobylinski RW, Zatz SL. In-
creased cholecystectomy rate after the introduction of laparoscopic cho-
lecystectomy. JAMA 1993; 270:1429-1432.
8. McMahon AJ, Fischbacher CM, Frame SH, MacLeod MC. Impact of
laparoscopic cholecystectomy: a population-based study. Lancet 2000;
356:1632-1637.
9. Richards C, Edwards J, Culver D, Emori TG, Tolson J, Gaynes R. Does
using a laparoscopic approach to cholecystectomy decrease the risk of
surgical site infection? National Nosocomial Infections Surveillance Sys-
tem, Centers for Disease Control and Prevention. Ann Surg 2003; 237:
358-362.
10. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline
for prevention of surgical site infection, 1999. Hospital Infection Control
Practices Advisory Committee. Infect Control Hosp Epidemiol 1999; 20:
250-278.
11. National Nosocomial Infections Surveillance (NNIS) system report, data
summary from January 1992 through June 2004, issued October 2004.
Am J Infect Control 2004; 32:470-485.
12. Ishizaki Y, Miwa K, Yoshimoto J, Sugo H, Kawasaki S. Conversion of
elective laparoscopic to open cholecystectomy between 1993 and 2004.
Br J Surg 2006; 93:987-991.
Are We “Squeezing The Balloon” When
Reducing the Risk of Occupational
Infection? Reply to Pan et al.
t o t h e e d i t o r — Under a witty title, Pan et al.1 described
a needlestick injury that occurred while a cytopathologist was
performing fine-needle aspiration cytology (FNAC) using the
modified method that I and my colleagues proposed2 to elim-
inate the needle manipulation involved in classical FNAC.
They relate that the needle shot out when the cytopathologist
depressed the plunger to extract the material obtained by
aspiration, and they suggest a possible cause: the needle was
clogged by a colloidal clot aspirated from a thyroid nodule.
Unfortunately, the needle bounced and lodged in the cyto-
pathologist’s scalp. With no other argumentation, they as-
sume that clot aspiration is inherent to the modified method
of FNAC and so is a new injury risk associated with use of
the modified method.
I agree that a clot might have clogged the needle and caused
the accident. Nevertheless, I don’t know the physical law that
explains why aspiration of a clot is only possible when using
the modified FNAC technique and not when using the con-
ventional FNAC method. Also, the reason for which the nee-
dle’s odd flight path and its unlucky ending must be consid-
ered an exclusive result of the modified FNAC method eludes
me. My personal experience includes more than 6,500 FNAC
procedures, more than 3,500 of which were performed with
the modified method. Although I cannot determine the exact
number, I have had a few experiences with both classical and
modified FNAC in which the needle shot out suddenly when
I depressed the plunger. Fortunately, no injury ever followed.
Finally, I don’t see the line of argument by which Pan et
96 infection control and hospital epidemiology january 2008, vol. 29, no. 1

al.1 conclude that reporting a diagnostic method that, with
no loss of effectiveness, permits us to eliminate needle ma-
nipulation and hence, to reduce the risk of injury, is equiv-
alent to “squeezing the balloon.” Again, I am in perfect agree-
ment with Pan et al.1 when they recommend that we use our
heads to perform FNAC safely. However, and to avoid mis-
understandings, I would dare to specify their advice further,
adding that, if possible, we shouldn’t use our scalps, but we
should make use of our common sense.
Ignacio Galed Placed, MD
From the Servicio de Anatomia Patologica, Seccion de Citologia, Hospital
Juan Canalejo, La Coruna, Spain.
Address reprint requests to Ignacio Galed Placed, MD, Servicio de
Anatomia Patologica, Seccion de Citologia, Hospital Juan Canalejo, Xubias
de Arriba 84, La Coruna, Spain, (Ignacio_Galed@canalejo.org).
Infect Control Hosp Epidemiol 2008; 29:95-96
䉷 2007 by The Society for Healthcare Epidemiology of America. All rights
reserved. 0899-823X/2008/2901-0021$15.00. DOI: 10.1086/524914
re f e re n c e s
1. Pan A, Signorini L, Magri S, De Carli G. Scalp needlestick injury during
fine-needle aspiration cytologic evaluation without needle manipulation:
William Tell in the laboratory, not quite. Infect Control Hosp Epidemiol
2006; 27:996.
2. Galed-Placed I, Pertega-Diaz S, Pita-Fernandez S, Vazquez-Martul E. Fine
needle aspiration cytology without needle manipulation to reduce the risk
of occupational infection in healthcare personnel. Infect Control Hosp
Epidemiol 2005; 26:336.

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