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Cellulitis in Obesity: Adverse Outcomes Affected by Increases in Body Mass

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DOI: 10.1177/2150131915583659 · Source: PubMed

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583659
research-article2015
JPCXXX10.1177/2150131915583659Journal of Primary Care & Community HealthTheofiles et al

Original Research
Journal of Primary Care & Community Health

Cellulitis in Obesity: Adverse

2015, Vol. 6(4) 233­–238
© The Author(s) 2015
Reprints and permissions:
Outcomes Affected by Increases in sagepub.com/journalsPermissions.nav
DOI: 10.1177/2150131915583659

Body Mass Index jpc.sagepub.com

Meghan Theofiles1, Julie Maxson1, Lori Herges1, Alberto Marcelin2,

and Kurt B. Angstman1

Abstract
Purpose: Cellulitis in obese patients is associated with increased rates of treatment failure compared to those with
normal body mass index (BMI); however, patients have not been extensively studied in the outpatient environment or
stratified based on range of obesity and associated risk factors. This study looked at antibiotic dosing and treatment
failure in the obese population from the primary care perspective and accounts for BMI range, weight, comorbid diabetes,
and tobacco use. Methods: This study was a retrospective chart review of 637 adult primary care patients designed to
evaluate rates of treatment failure of outpatient cellulitis among patients of varying BMI. Treatment failure was defined as
(a) hospital admission for intravenous antibiotics, (b) prolonged antibiotic course, or (c) requiring a different antibiotic after
initial course. Results: Adverse outcomes were not statistically significant between normal BMI and those with BMI ≥40
kg/m2. A subset of patients with a BMI ≥50 kg/m2 was noted to have approximately twice the rate of adverse outcomes
as the normal BMI group. While controlling for age, gender, race, diagnosis of diabetes mellitus, and tobacco use, a BMI of
≥50 kg/m2 and a weight ≥120 kg was associated with adverse outcomes with an odds ratio of 2.440 (95% CI, 1.260-4.724;
P = .008) and 2.246 (95% CI, 1.154-4.369; P = .017), respectively. Conclusions: Patients with cellulitis weighing >120kg
or with a BMI ≥50 kg/m2 were at greatest risk for treatment failure in the outpatient setting, even when controlling for
comorbid diabetes and tobacco use. As morbid obesity continues to become more prevalent, it becomes imperative that
primary care physicians have better antibiotic dosing guidelines to account for the physiologic effects of obesity to minimize
the risk of increased morbidity, health care costs, and antibiotic resistance.

Keywords
primary care, diabetes, tobacco use

Introduction guidelines for cefepime, cefazolin, and ciprofloxacin in

Obesity is now recognized by the World Health Organization
as a global pandemic spanning all socioeconomic classes
with a projected 700 million affected by 2015. An alarming
one-third of Americans are obese, with 1 out of 20 meeting
criteria for morbid obesity (body mass index [BMI] ≥40
kg/m2).1 From a public health standpoint, this raises serious
concerns about associated morbidity and mortality, includ-
ing increased risk of infection in this population. Not only
has obesity been shown to be a predisposing factor in
acquiring infections, but it also results in worse clinical out-
comes than in patients with normal BMI.2 Despite the
increasing prevalence of obesity, there are few guidelines
for antimicrobial dosing in obese patients and poor adher-
ence to those already in place. In a recent retrospective
study in the emergency department setting, emergency phy-
sicians adhered to their institution’s weight-based antibiotic
8.0%, 3.0%, and 1.2%, respectively.3
Several studies have addressed antimicrobial dosing con-
siderations in obese patients. Although the absorption of
drugs does not seem to be significantly modified in obesity,
the processes of volume of distribution (Vd), protein binding,
metabolism, and antibacterial clearance are significantly
altered.4 According to Food and Drug Administration regu-
lations, pharmaceutical companies are required to demon-
strate average population effectiveness for new antimicrobial
1
Mayo Clinic, Rochester, MN, USA
2
Mayo Clinic Health System, Austin, MN, USA
Corresponding Author:
Meghan Theofiles, Department of Family Medicine, Mayo Clinic, 200
First Street SW, Rochester, MN 55905, USA.
Email: theofiles.meghan@mayo.edu
234 Journal of Primary Care & Community Health 6(4)
agents including children, the elderly, and those with renal
and hepatic impairment. However, effectiveness data for
those of higher than normal BMI are not required leading to
underrepresentation of the obese population.5 For primary
care providers, this is of particular concern, as they serve on
the frontline in administering antibiotics for most outpatient
infections. Without appropriate data and guidelines to direct
antibiotic treatment in the growing obese population, inad-
equate dosing is likely contributing to treatment failure,
unnecessary escalation to broader spectrum antibiotics, and
selection of resistant pathogens in obese patients.
Cellulitis is one of the most common bacterial infections
seen in the primary care setting, with an incidence that has
increased from 8.6 million to 14.2 million from 1997 to
2005.6 From a recent retrospective analysis, both morbid
obesity and inadequate empiric antibiotic therapy were
independent risk factors for treatment failure in hospitalized
patients with cellulitis (odds ratio 4.10, P = .02; and odds
ratio 9.25, P < .01, respectively).7 However, little is known
about the relationship between specific BMI categories and
weight with treatment failure in patients with skin and soft
tissue infections. There is a need for more BMI-specific rec-
ommendations regarding antimicrobial dosing for patients
>120 kg and normal organ function; such recommendations
might include modified dosing for beta-lactams, trime-
thoprim-sulfamethoxazole, and many intravenous antibiot-
ics. Many recommendations may be based on the available
pharmacokinetic properties of the drug and the frequency
and severity of known toxicities rather than published
research studies.
For adult patients diagnosed with cellulitis in the pri-
mary care setting, we hypothesized that an increased BMI
would correlate with adverse outcomes (specifically, pro-
longed antibiotic course, escalation of antibiotic choice, or
hospitalization for intravenous administration of antibiot-
ics). Since other factors such as the diagnosis of diabetes
and tobacco use may be confounding issues, these condi-
tions will specifically be controlled for in this study. With a
recent (2014) institutional guideline suggesting increased
doses for antibiotics in patients weighing more than 120 kg,
we used weight in a secondary analysis.
Methods
This was a retrospective study involving primary care
patients within a Mayo Clinic setting located in the Midwest.
All patients who had a primary diagnosis of cellulitis from
June 2008 through June 2013 were identified using ICD-9
(International Classification of Diseases, ninth revision)
codes. After approval by the organization’s institutional
review board, adult patients were screened and only those
having given prior research authorization were included.
Data were collected using both automated and manual pro-
cesses. Demographic data recorded included age, gender,
and race. Clinical data abstracted included height, weight,
BMI, recent tobacco use, comorbid diagnosis of diabetes,
antibiotic prescribed/ treatment methods used, and dosing.
Any cellulitis case in which the patient was directly admit-
ted to the hospital for treatment after being initially diag-
nosed was excluded from the analysis, as the focus of the
study was outpatient management of cellulitis. Medical
records with an obvious error in documentation (usually
BMI) were also screened and removed.
Much of the data was retrieved using automated queries.
However, because of limitations of the program, the data
regarding each provider’s method or choice of treatment,
including medication type, dose, and duration were manu-
ally abstracted by a family medicine resident and clinical
research coordinator. The medical charts were also manu-
ally reviewed to determine smoking status within the previ-
ous 12 months.
We compared a cohort of patients with BMIs at 40 kg/m2
and higher with a cohort of age-and gender-matched con-
trols having BMIs in the range of 18.5 to 25 kg/m2 at the
time of their cellulitis diagnosis. The dependent variable
was treatment failure as defined by (a) hospital admission
for intravenous administration of antibiotics and (b) pro-
longed therapy (defined as an extended course of the initial
antibiotic or a different antibiotic after initial course was
completed.
Student’s t test was used for statistical analysis of the
continuous variable. Categorical data were analyzed with
chi-square testing. Multiple logistic regression modeling
for the clinical outcome of an adverse outcome of either
hospitalization or prolonged treatment within 30 days of the
diagnosis of cellulitis as an outpatient was performed while
retaining all independent variables studied. Statistical sig-
nificance was set at P < .05. Calculations were performed
on MedCalc software (www.medcalc.org, version 14.10.2).
Results
Of the 637 patients in the study cohort, 393 (61.7%) were of
a BMI ≥40.0 kg/m2 and 244 (38.3%) were of normal BMI.
Between the 2 groups of patients, those with a normal BMI
were younger, more likely white women without diabetes
and weigh less than 120 kg (Table 1). There was no differ-
ence between the 2 groups of patients with regard to tobacco
use, which ranged from 16.5% to 19.1%. Overall, adverse
outcomes were not statistically significant between the
groups, with almost 1 in 5 patients experiencing either a
prolonged therapy or hospitalization for their cellulitis.
While hospitalizations were approximately 1 in 20 from
each group; approximately 20% (range 17.9% to 19.6%)
required prolonged or altered therapy.
With subgroup analysis of the BMI ≥40 kg/m2 group, the
patients with a BMI of 40 to 50 kg/m2 had similar adverse
events compared with patients with a normal BMI; while
Theofiles et al 235

Table 1.  Demographics and Clinical Factors by Body Mass Index (BMI; Normal vs ≥40 kg/m2) of Primary Care Patients Diagnosed
With Cellulitis as an Outpatient, by Variable.

BMI ≥ 18.5 to <25 kg/m2

(N = 244) BMI ≥ 40.0 kg/m2 (N = 393) P
Age, years 48.2 (19.0-82.0) 52.0 (19.0-97.0) .004
Gender, % female (n) 76.2 (186) 64.1 (252) .002
Race, % white (n) 98.7 (221) 95.4 (375) .02
Weight >120 kg, % (n) 0.0 (0) 64.4 (253) <.001
Diabetes, % yes (n) 8.9 (20) 37.7 (148) <.001
Tobacco use, % (n) 16.5 (37) 19.1 (75) .248
Adverse outcome, % (n) 17.9 (40) 20.1 (79) .268
Hospitalization, % (n) 4.5 (11) 6.6 (26) .348
Prolonged therapy, % (n) 17.9 (40) 19.6 (77) .341

Percentage of Adverse Events by BMI

p=0.008
40.00%
35.10%
35.00%

30.00% 28.60%

25.00%

20.00% 17.90% 17.20%

15.00%

10.00%

5.00%

0.00%
18.5-25 (N=244) 40-50 (N=322) 50-60 (N=57) >60 (N=14)

Figure 1.  Percentage of adverse events (either hospitalization or prolonged therapy) for outpatient patients diagnosed with cellulitis,
by body mass index (BMI) category.

the patients with a BMI ≥50 kg/m2 were noted to have
almost twice the rate of adverse outcomes as the normal
BMI group and the subgroup of patients with a BMI of ≥40
to <50 kg/m2 (Figure 1). These 71 patients with “super obe-
sity” were almost all more than a weight of 120 kg (98.6%)
and had a much higher incidence of diabetes when com-
pared with the patients with normal BMI (40.8% vs 4.9%,
P < .001; Table 2). Adverse outcomes were noted in 33.8%
of these patients compared with 17.9% of the normal BMI
patients. There were no demographic statistically signifi-
cant differences noted between these 2 groups of patients
for age, gender, race, or tobacco use.
Using a logistic regression analysis for presence of an
adverse outcome within 30 days of the diagnosis of outpa-
tient cellulitis in the cohorts of the 71 patients with BMI
≥50 kg/m2 and 244 patients with a normal BMI (N = 315)
while retaining all the demographic variables, a BMI of ≥50
kg/m2 was associated with an odds ratio of 2.440 (95% CI,
1.260-4.724; P = .008) and weight >120 kg was associated
with an odds ratio of 2.246 (95% CI, 1.154-4.369; P = .017;
Table 3). Age, gender, race, the diagnosis of diabetes mel-
litus, or the use of tobacco were not associated with a wors-
ening outcome of cellulitis, when controlling for all other
variables for either model.
Discussion
In this study, we determined rates of treatment failure in
patients initially diagnosed with cellulitis in the outpatient
setting with a particular emphasis on specific ranges of
236 Journal of Primary Care & Community Health 6(4)

Table 2.  Demographics and Clinical Factors by Body Mass Index (BMI; Normal vs ≥50 kg/m2) of Primary Care Patients Diagnosed
With Cellulitis as an Outpatient, by Variable.

BMI ≥18.5 to <25.0 kg/2

(N = 244) BMI ≥ 50.0 kg/m2 (N = 71) P
Age, years 48.2 (19.0-82.0) 47.4 (19.0-82.0) .717
Gender, % female (n) 76.2 (186) 66.2 (47) .123
Race, % white (n) 98.7 (221) 94.45 (67) .445
Weight >120 kg, % (n) 0.0 (0) 98.6 (70) <.001
Diabetes, % yes (n) 8.9 (20) 40.8 (29) <.001
Tobacco use, % (n) 16.5 (37) 22.5 (16) .200
Adverse outcome, % (n) 17.9 (40) 33.8 (24) .002
Hospitalization, % (n) 4.5 (11) 12.7 (9) .027
Prolonged therapy, % (n) 17.9 (40) 33.8 (24) .002

Table 3.  Odds Ratios for Adverse (Either Prolonged Treatment or Hospitalization) Event Within 30 Days of Diagnosis of Cellulitis
(for Normal Body Mass Index [BMI] Patients vs BMI ≥50 kg/m2) by BMI or Weight, by Variable (N = 315).

Odds Ratio 95% CI P

BMI
 Age 1.001 0.983-1.020 .889
  Gender (female) 0.869 0.463-1.628 .660
  Race (white) 0.821 0.308-2.185 .692
  Diabetes (yes) 1.152 0.523-2.534 .726
  Tobacco use (yes) 1.255 0.607-2.596 .540
 BMI ≥50 kg/m2 2.440 1.260-4.724 .008
Weight
 Age 1.009 0.982-1.020 .931
  Gender (female) 0.853 0.456-1.597 .620
  Race (white) 0.833 0.314-2.213 .714
  Diabetes (yes) 1.194 0.543-2.627 .660
  Tobacco use (yes) 1.262 0.611-2.605 .530
  Initial weight >120 kg 2.246 1.154-4.369 .017

obesity, including morbid obesity (BMI 40-50 kg/m2) and
super obesity (BMI ≥50 kg/m2). We were surprised to see
minimal differences in the rates of prolonged antibiotic
therapy and hospitalizations between normal BMI and the
BMI 40 to 50 kg/m2 cohort; however, the rates of adverse
outcomes in the BMI ≥50 kg/m2 cohort was quite marked
and independent from other studied variables including age,
gender, comorbid diabetes, and tobacco use. It was observed
that most patients within this latter group had a weight of
>120 kg, suggesting a weight at which concerns for inade-
quate antibiotic therapy should be triggered. This study
adds to the knowledge base of outpatient treatment for cel-
lulitis in patients with obesity, by controlling for the poten-
tial confounding factors of diabetes mellitus and tobacco
use. Also, the significant change in adverse events at BMIs
≥50 kg/m2 vs BMI of 40 to 50 kg/m2 was intriguing, as prior
studies have not subcategorized BMIs >40 kg/m2.
With these findings in mind, current prevalence data
have shown that the highest BMI groups are increasing at
the fastest rates. From a period of 2000 to 2005, self-
reported BMI higher than 40 kg/m2 increased by 50% with
BMI >50 kg/m2 increasing by 75%, approximately 3 times
the rate of moderate obesity.8 Based on obesity trends in
Pennsylvania school children from 2007 to 2011, Lohrmann
et al9 project the prevalence of overweight, obesity, and
extreme high obesity of Pennsylvania school children to be
16%, 6.6%, and 23% by 2031, lending additional evidence
that morbid and severe obesity are surpassing general trends
in moderate obesity. As clinically severe obesity continues
to become a significant portion of the nation’s weight distri-
bution, we will undoubtedly see more clinically relevant
ramifications especially in terms of drug dosing.
From a pharmacologic standpoint, differences in drug
metabolism among obese individuals have drawn signifi-
cant attention over the past decade and are well described in
the literature, although clinical evidence has lagged behind.
In general, oral absorption may play a minor role in
decreased drug concentrations due to delayed gastric
Theofiles et al 237
emptying commonly seen in obesity. Volume of distribution
(Vd), however, is significantly altered in obesity compared
with normal-weight individuals. In terms of lipophilic anti-
biotics (eg, fluoroquinolones and macrolides), Vd is typi-
cally increased in obesity due to increases in adipose tissue.
Additionally, Vd in hydrophilic antibiotics (eg, beta-lactams
and aminoglycosides) is also increased with water compris-
ing 30% of adipose tissue thus increasing lean body weight.
Less is known about hepatic metabolism, although fatty
infiltration of the liver and increased activity of the cyto-
chrome P450 pathway has been implicated in altered
metabolism. Glomerular filtration rate has been shown to be
increased in obese individuals if otherwise healthy. Those
with associated comorbidities such as hypertension and dia-
betes can have significantly impaired renal function posing
risk for toxicity with increased antibiotic dosing.4,10,11
Reaching target antimicrobial concentrations in obese
individuals has proven to be complex and certainly warrants
additional clinical investigation. However, a few general con-
siderations have been recognized which are reflected in our
institutional guidelines for antimicrobial dosing in obesity. In
general, penicillins and cephalosporins are suggested to be
used at the higher end of suggested dosage range because of
the relatively low rate of toxicity and adverse effects.11 In a
recent study looking at cefazolin concentrations in adipose tis-
sue at surgical sites, cefazolin concentrations were shown to
be inversely proportional to BMI (r = −0.67, P < .001) with a
significant proportion of obese and extremely obese not
achieving minimal inhibitory concentrations for Gram-
negative rod coverage in adipose samples at 20% and 33.3%,
respectively.12 In a commonly cited study, Forse et al13 showed
that increasing cefazolin from 1 to 2 g resulted in 75% to
100% increase in tissue concentrations and resulted in a sig-
nificant reduction in surgical site infections from 16.5% to
5.6%. Rather than using the higher end of dosage range for
cephalosporins, our institutional guidelines as of July 2014,
simply recommend doubling the dose in patients weighing
greater than 120 kg with no known organ dysfunction.
Our findings support the recent update in our institu-
tional guidelines directing providers to increase specific
antibiotics such as penicillins and cephalosporins in patients
weighing greater than 120 kg. Our data were collected from
clinical episodes spanning from 2008 to 2012, predating
these guidelines, with the vast majority of the patients
included receiving cephalexin at standard dosing of 500 mg
orally 3 to 4 times per day. It would be interesting to com-
pare future rates of treatment failure with the new guide-
lines in place as well as rates of adherence among providers.
Our data assessed risk of treatment failure in the outpatient
setting and cannot be generalized to the inpatient setting.
Another study showed weights of just 100 kg and BMI of
>40 kg/m2 significantly associated with clinical failure in
hospitalized patients with cellulitis.7 We too may have had
similar findings if we assessed clinical failure once patients
reached the inpatient setting. These findings are also appli-
cable to the dosing of antibiotics for prophylaxis of recur-
rent cellulitis. The PATCH I trial found that BMI >33
kg/m2, lymphedema, and multiple previous episodes were
independent risk factors for failure of penicillin prophylaxis
and that the increased prophylaxis failure rate in obese
patients may be linked to underdosing of penicillin for
BMI.14
There were several limitations to this study with the
most obvious being our reliance on the clinical diagnosis of
cellulitis. Misdiagnosis of noninfectious conditions like sta-
sis dermatitis as cellulitis is a common error, occurring as
often as 28% in a recent study performed at University of
California Los Angeles Medical Center.15 This was mini-
mized by excluding cases where there was a high degree of
diagnostic uncertainty, but again we relied on accurate and
detailed charting to do this. In an attempt to keep our study
generalizable, we did not account for comorbid chronic
medical conditions (chronic obstructive pulmonary disease,
chronic kidney disease, cancer, etc),preexisting stasis der-
matitis, chronic lymphedema, or immunocompromised sta-
tus which may have an impact on cellulitis outcomes and
could be considered for a future analysis. We also may have
gleaned useful information from recording the mechanism
of infection, as bites and trauma can predispose to infection
of deeper structures that are more difficult to treat. There
were also challenges in determining what defined prolonged
treatment. If patients were found to have an allergic reaction
to the medication initially prescribed, another medication
was often prescribed in its place, thus extending the dura-
tion by several doses and days. This example was not coded
as a prolonged therapeutic treatment, however, not all medi-
cation changes were as well documented leading to possible
misinterpretation.
In addition, not all BMI categories were evaluated in this
study. It was demonstrated in our study that there was no
difference in the adverse outcomes noted between patients
with a normal BMI and those of a BMI of 40 to 50 kg/m2
and that the difference in outcomes was only associated
with those of a BMI >50 kg/m2 compared with a normal
BMI. Our study was designed to compare those that would
be eligible to require antibiotic dosing changes (BMI >40
kg/m2) and those who did not (BMI 18.5-25.0 kg/m2). Also,
we did not determine the retrospective control of the
patient’s diabetes at the index by determining the most
recent hemoglobin A1c. Diabetes control would be best
determined by an A1c at index date or within two months
prior and we felt this would be best determined by a poten-
tial prospective analysis of cellulitis in diabetic patients.
Retrospective data may or may not have been available, and
would have diminished the potential number of diabetic
patients.
238 Journal of Primary Care & Community Health 6(4)
Conclusions
Patients with BMI >50 kg/m2 and weight >120 kg have
increased rates of antibiotic treatment failure, even when
controlling for comorbid diabetes or tobacco use.
Additionally, both adults and children with BMI >50 kg/m2
are growing faster than any other subset of obese patients.
This highlights the need for increased provider awareness
of dosing requirements in this population as well as contin-
ued research to support current guidelines and promote
additional recommendations for oral antibiotics beyond
beta-lactams.
Authors’ Note
Departmental resources were used for this study. All authors were
involved in writing the article and had final approval of the sub-
mitted and published versions.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article.
Funding
The author(s) disclosed receipt of the following financial support
for the research, authorship, and/or publication of this article:
Department of Family Medicine, Mayo Clinic, Rochester,
Minnesota.
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Author Biographies
Meghan Theofiles, MD, is a PGY-3 resident at Mayo Family
Medicine Residency Program in Rochester, MN. Her clinical
interests include obesity, weight management, and women’s
health.
Julie Maxson, BA, is a clinical research coordinator for the
Department of Family Medicine at Mayo Clinic in Rochester,
Minnesota. Her research interests include obesity prevention, spe-
cifically promoting healthy habits in regard to nutrition and exer-
cise. She is also interested in the study of new diagnostic tools
which may lead to practice-changes in the clinical setting.
Lori Herges, Pharm D, is an instructor in Pharmacy at Mayo
Clinic in Rochester, Minnesota. She is a clinical pharmacist serv-
ing Family Medicine and Cardiology. Her clinical interests include
infectious diseases and cardiology.
Alberto Marcelin, MD, is a family medicine physician within the
Mayo Clinic Health System and clinical associate at Mayo Clinic
in Rochester, MN. His interests included travel medicine, infec-
tious diseases, and obesity.
Kurt B. Angstman, MS, MD, is an associate professor of Family
Medicine at Mayo Clinic in Rochester, Minnesota. He is a core
faculty of the Family Medicine Residency Program. His clinical
interests include depression care management for depression and
practice improvement.