Infection of Penile Prostheses in Patients with Diabetes Mellitus

Abstract

Background:

Controversy still exists in some centers on whether diabetes mellitus is a risk factor for penile prosthesis infection. The aim of this review is to examine the evidence correlating penile implant infections to the presence of diabetes mellitus in patients with organic erectile dysfunction.

Methods:

We performed a systematic review searching through Medline database from 1960 to 2014, using keywords; penile prosthesis(es), penile implant(s), and diabetes mellitus. We used the Prisma 2009 Flow diagram for systematic reviews. Thirty-eight publications were selected for inclusion in this qualitative analysis.

Results:

Most case series reporting a greater infection rate in patients with diabetes mellitus date from the 1970s to 1990s. These series reported an infection rate of 5.5 to 20% and contained small cohort of patients. In the 1990s larger case series reported a lower infection rate in patients with diabetes mellitus compared with patients with paraplegia, pelvic trauma, and patients on steroids, but still reported an infection rate as high as 10.6%. With the implementation of antibiotic coated implants in 2001, infection rates reduced further with reported rates becoming less than 2% in patients with diabetes mellitus. The latest and largest case series by Eid et al. (2012) reported an infection rate of 0.46% with antibiotic coated implants and “no touch” technique in a cohort of 1511 cases, out of which 41% were patients with diabetes mellitus.

Conclusion:

Strong evidence exists that the risk of penile prosthesis infection has reduced over the decades with device improvement and surgical expertise. In larger case series infection rates in patients with diabetes mellitus is not statistically significant from that experiences in the population at large.

Erectile dysfunction is defined as the inability to achieve or maintain an erection sufficient to engage in sexual intercourse to the satisfaction of both partners. Organic erectile dysfunction implies an endocrine, vascular, or neurological basis or a combination of these factors that interferes with the normal physiology of the penis [1]. One of the most disturbing complications of diabetes mellitus in men is erectile dysfunction with a reported incidence up to 50% [1,2].

Penile implants or prostheses are generally considered a “last resort” management option in patients whose erectile dysfunction has an organic cause and who are unwilling to consider, fail to respond to, or are unable to continue with medical treatment or external devices. Such prostheses are malleable, semi-rigid, or inflatable implants, which are surgically inserted into the penis to allow an erect state. Disadvantages though do exist, e.g., invasiveness of procedure, infection or erosion of implant, mechanical problems with the device and in some cases chronic pain [2,3].

The earliest reports of penile implants being used for the treatment of diabetic erectile dysfunction date from the 1960s. Behairi introduced the synthetic rods in 1960 and the inflatable penile prosthesis was introduced by Scott in 1973. The hydraulic two-piece and three-piece implants have become the most popular in our current practice providing a more natural flaccid appearance and erection [2,4]. Since then, improvements in the design of the prosthesis have evolved and in the last decade a new antibiotic-coated inflatable penile prosthesis has been introduced, which includes a surface layer impregnated with antibiotics to further reduce the incidence of infection [5,6].

Aims

Despite the above improvements, infection of the prosthesis still remains the most substantial complication in penile implant surgery. The primary objective of this review was to determine whether the presence of diabetes mellitus increases the risk of penile prosthesis infection compared with those patients without diabetes mellitus.

Patients and Methods

We performed a systematic review and identified the literature to be included using the Prisma 2009 Flow Diagram [7]. We performed a search through Medline database from 1960 until 2014 using the keywords: Penile; implant; prosthesis and diabetes mellitus. One hundred sixty articles were identified through Medline database search and 29 additional articles from other sources. One hundred articles were excluded after initial screening as were not relevant to the study. Eighty-nine full articles were assessed for eligibility and 51 articles were excluded further as the diabetic group was not specified and not relevant to primary outcome. Thirty-eight studies were included for qualitative analysis.

Most studies found in the literature search were case series therefore level of evidence 4 [Oxford Centre for Evidence Based Medicine (OCEBM)] [8]. An independent reviewer participated in the selection of articles for the systematic review to reduce selection bias.

Results

We reviewed, in total, 38 case series that reported their outcomes of penile prosthesis in patients with diabetes mellitus. To make evaluation easier we divided the publications into the following three categories.

1. Case series indicating that penile prosthesis infection is greater in patients with diabetes mellitus,

2. Case series with supportive evidence of greater rate of penile prosthesis infection in patients with co-morbidities other than diabetes mellitus, and

3. Case series reporting no statistically significant raised infection rate in patients with diabetes mellitus receiving a penile prosthesis.

Case series reporting that penile prosthesis infection is greater in patients with diabetes mellitus (Table 1)

Diabetes mellitus is an endocrine disease affecting multiple organs simultaneously. Patients with diabetes mellitus may be more susceptible to infection physiologically because of altered defense mechanisms, secondary to polymorphonuclear leukocyte dysfunction, and decreased phagocytic and bactericidal activity. In addition to this, microangiopathy decreases delivery of monocytes and polymorphonuclear leukocytes at the site of infection [9].

Table 1.

Studies Reporting Higher Rates of PP Infection in Patients with DM

First author/Year	Time scale	Type of prosthesis	Number of subjects	Number of diabetic patients	Infection rate in diabetic patients	Infection rate in non-diabetics	Infection rate—Group not specified
Wilson (1988) [26]	1974–1984	Inflatable	395	20%	Report higher		3.5%
Cumming et al. (1991) [27]	1983–1987	MalleableInflatable	13011020	33 (25%)	20%	10% in neurogenic
Bishop et al. (1992) [28]	1987–1988	Prosthesis not specified	90	36%	5.5%	0%
Wilson et al. (1998) [9]	1994–1996	Two-piece IPP	389	114 (29.3%)	8.8%	4.0%
Cakan et al. (2003) [29]	1993–2000	Malleable two-pieceSelf-contained	135115812	47	10.6%	15% in paraplegics
DiBlasio et al. (2010) [30]	1997–2007	Inflatable	79	43 (54%)	9.3%	2.7%
Mulcahy et al. (2011) [31]	2001–2008	Non-impregnated two-pieceM/R impregnated two-piece	--	6246,071	4.17%1.47%	Overall1.53%Vs 1.88%In DM	-

IPP = inflatable penile prosthesis; M/R = minocycline HCL-rifampicin; DM = diabetes mellitus; PP = penile prosthesis.

Infection of a prosthesis is defined as swelling or discharge of pus requiring surgical attention associated with the growth of a specific organism. This can be a disastrous complication, resulting in removal of the implant, loss of function, and difficult device replacement [10].

Earlier case series dating from the 1970s concluded that diabetes mellitus was an important risk factor for penile prosthesis infection. We have found 15 case series from our literature search that have reported this outcome, but unfortunately this was without robust supportive evidence. These were small series in an era where both malleable and inflatable penile prostheses were implanted and high complication rates were reported [11 –23]. Some of these studies even lack data and patient demographics. We have identified two case series, one by Small et al. in 1976, who reports a non-existent complication rate in 13 patients with diabetes mellitus receiving a Small-Carrion penile prosthesis and Morales et al. in 1973, who reported implant infection in two out of five patients with diabetes mellitus [24,25].

Wilson et al. in 1988 published their outcomes of inflatable penile prostheses implantation in 395 consecutive patients where the original AMS system resulted in a 61% complication and revision rate over a follow-up period ranging from 3 to 11 y. In the same series, newer prosthesis implanted since 1983 had a lower 13% revision at 4 y of follow-up. A greater infection rate was reported in patients with diabetes mellitus but more detailed analysis was unavailable. This reduction in the rate of infection was reported to be as a direct consequence of increased operative speed, double gloving, and use of sterile drape material preventing the drapes becoming soaked from the frequent antibiotic irrigant [26].

In 1991 Cumming et al. report on 130 patients who received penile prostheses, mostly malleable from 1983 to 1987. Although the overall infection rate was 10%, this doubled to 20% for their cohort of 30 patients with diabetes mellitus [27].

A year later, Bishop et al. reported on the utilization of glycosylated hemoglobin in patients with diabetes mellitus to estimate correlation with subsequent risk of implant infection. They performed an 18-mo prospective study of 90 patients undergoing penile prosthesis implantation. Of these 90 patients, five experienced periprosthetic infection (5.5%) requiring removal of the device and all infections occurred in the patients with diabetes mellitus corresponding to a rate of 36% amongst this group. Of the patients with diabetes mellitus, 41.4% had poorly controlled diabetes mellitus with a glycosylated hemoglobin concentration of greater than 11.5% and 80% of the infections occurred within this group. Therefore, Bishop et al. calculated a risk of infection of 31% in patients with poorly controlled diabetes mellitus versus 5% of the adequately controlled group. As a consequence of this study the authors changed their practice to postponing penile prostheses in cases with poorly controlled diabetes mellitus [28].

Wilson et al. attempted in 1998 to quantify the risk of infection in patients with elevated glycosylated hemoglobin. They performed a 2-y prospective study of 389 patients, 114 of which had diabetes mellitus and their results did not show a statistically significant increase in prosthesis infection with increased concentrations of glycosylated hemoglobin. They suggested that the most important prognostic factor was the duration of diabetes mellitus rather than its control with a 4.4% greater risk of infection in patients with diabetes mellitus compared with those without [9].

It is worth mentioning that in 2003, even though Cakan M reports in his case series of 135 cases that only paraplegia increased the risk of infection he also found that prosthesis infection incidence increased when fasting glucose concentration was more than 200 ng/mL and 10.6% of their group with diabetes mellitus presented with infection [29].

In a smaller series on 79 patients by DiBlasio et al., they reported that Peyronie's disease was the only substantial predictor of component malfunction on both univariate and multivariable analysis when adjusting for age, BMI, diabetes mellitus, and tobacco use. They reported five patients with inflatable penile prosthesis infections requiring removal of prosthesis, four of whom had diabetes mellitus representing an infection rate of 5% over a mean follow-up of 19.6 mo [30].

In 2011, Mulcahy et al. reviewed infection related revisions for minocycline HCL-rifampicin (InhibiZone) impregnated and non-impregnated implants. They identified 6071 patients with diabetes mellitus in the InhibiZone group and 624 patients with diabetes mellitus in the non-impregnated group. Initial revisions because of infection were reported for 1.47% of M-R-impregnated versus 4.17% of non-impregnated implants. At 7 y the rate of infection-related revisions was substantially lower for InhibiZone implants. Also they report a substantially greater rate for revisions because of infection at 7 y for men with diabetes mellitus (1.88% compared with 1.53%). Despite this, there is no report of an association of infection with hematoma formation or erosion in this retrospective data analysis from a commercial database. In addition, the exact details regarding antibiotic prophylaxis, surgical technique and surgeon experience were not reported. This, however is the most recent case series that supports a greater infection rate in patients with diabetes mellitus [31].

Case series with supportive evidence of greater rate of penile prosthesis infection in patients with other co-morbidities other than diabetes mellitus (Table 2)

There have been many case series looking into the causes of penile prosthesis infection, challenging whether or not diabetes mellitus truly is a risk factor or whether high infection risk is actually attributed to other, more influential factors such as surgical technique and maintaining sterility intra-operatively.

Table 2.

Studies Reporting Higher Rates of PP Infection in Patients with Other Risk Factors

First author/Year	Time scale	Type of prosthesis	Number of subjects	Number of diabetic patients	Infection rate in diabetic patients	Infection rate in non-diabetics
Radomski et al. (1991) [32]	1979–1989	Semi-rigidInflatable	269162107	56	0.37%	1.48%Neurogenic Bladder
Wilson et al. (1995) [33]	1986–1993	Inflatable	823	125	3%	9% (SCI)50% (Steroid use)
Cakan et al. (2003) [29]	1993–2000	MalleableTwo-pieceSelf-contained	135115812	47	10.6%	15% in paraplegics
Minervini et al. (2005) [34]	1975–2000	MalleableTwo-pieceSelf contained	4823728030	115	12/115 (10%)	21% of men with pelvic trauma
Kim et al. (2010) [35]	1991–2009	AMS700CXAMS700CXM	397	113 (28.5%)	0.5%	0.75% patients on steroids
Paranhos et al. (2010) [36]	2001–2008	Malleable	139	63 (45.3%)		3.3 times higher post Radica Prostatectomy

SCI = spinal cord injury; PP = penile prosthesis.

Radomski reviewed 269 cases of penile implant insertion over a 10-y period and reported only six cases of infection, all of which had a history of urinary tract infection. Four patients had a history of neurogenic bladder and one had diabetes mellitus, representing an infection rate of 15% and 0.37%, respectively. In all 269 cases, they maintained a strict policy with perioperative prevention of infection with: Perioperative antibiotics, intra-operative shave and scrub, and strict surgical technique resulting in a low overall infection rate requiring prosthesis removal in only 1.9% [32].

Wilsons et al. retrospective review of 1337 consecutive inflatable prosthesis (823 primary prostheses and 514 revisions) included 125 patients with diabetes mellitus, 66 patients with spinal cord injury and 10 patients who used steroids in the primary prosthesis group. The infection rate in each group requiring removal of prosthesis was 3%, 9%, and 50% respectively. The overall infection rate in the revision group was 10%. Patients with diabetes mellitus had a greater rate of re-infection after re-implantation of prosthesis at 18%. Salvage operation at the stage of this review had not been fully developed and incorporated in the authors' practice and this could explain the high rates of re-infection whether the patients had diabetes mellitus or not [33].

In 2003 Cakan reported that in a cohort of 135 cases with penile prostheses, only paraplegia increased the risk of infection. This could be associated with a neuropathic bladder predisposing the patient to recurrent urinary tract infections supporting Wilsons findings in 1995 [29].

Whilst Minervini et al. reported no statistically significant increased infection in patients with diabetes mellitus having penile prosthesis insertion, they did report a statistically significant correlation between patients with a history of pelvic trauma and ruptured urethra with infection of prosthesis [34].

In other series, both Kim et al. and Paranhos et al. reported a lack of substantial difference in the prosthesis infection rate between patients with and without diabetes mellitus although other risk factors were identified as pre-operative steroid therapy and previous radical retropubic prostatectomy [35,36].

Case series with no statistically significant raised infection rate in patients with diabetes mellitus receiving a penile prosthesis (Table 3)

More contemporaneous series have indicated that the presence of diabetes mellitus does not substantially raise the infection rate of penile prosthesis implantation surgery. Potential causes for this are varied and include prosthesis design advances, introduction of antibiotic-coated prostheses, improvement of surgical technique, and high experience in centers of excellence.

Table 3.

Studies Reporting Non-Statistically Significant PP Infection Rate in Patients with DM

First author/Year	Time scale	Type of prosthesis	Number of subjects	Number of diabetic patients	Infection rate in diabetic patients	Infection rate in non-diabetics	Infection rate—Group not specified
Scott et al. (1980) [37]	1976–1979	Inflatable	50	100%	<2%
Carson (1983) [38]	1979–1982	Inflatable	100	25%	1%	0%
Sidi et al. (1987) [43]	1980–1985	MalleableInflatable	14	100%	0%
Choi et al. (1994) [39]	1983–1993	MalleableSelf-InflatableInflatable (two- and three-piece)	2951654466	22.4%	0%	0.67% pelvic trauma, Spinal injury
Anafarta et al. (1996) [40]	1989–1994	AMS DynaflexAMS MalleableAMS Ultrex	10439614	18 (17%)	0.96%	0%
Garber et al. (1998) [41]	7 y	Mentor A1 (3-piece IPP)	360primary	144 (40%)	2.8%	0.9%P:0.18
Montague et al. (2001) [42]	1986–1999	3 piece	491	137	2.2%	2%
Wilson et al. (2007) [10]	3 y	AMS700CX + InhibiZone	467–161 were revisions	83	1%	0% (223 non diabetics)
Eid et al. (2012) [44]	8.5 y	Non-coated IPPCoated IPPCoated “no touch” IPP	1327041,511	39%37.9%43%	21% of the infections were diabetics		5.3%2%0.46%
Chung et al. (2013) [45]	30 y	Ultrex Cylinder (516)CX Cylinders (259)	955	24%	2%	3.6% (pelvic trauma patients)
Song et al. (2013) [46]	10 y	Malleable (45)Two-piece inflatable (179)	224201 followed up	9 (4%)	1 case +erosion (0.5%)	0

IPP = inflatable penile prosthesis; PP = penile prosthesis.

In 1980, Scott et al. reported a low infection rate of <2% in a population of 50 patients with diabetes mellitus receiving a penile prosthesis. Despite the lack of a comparative group, this represented the lowest reported infection rate published at that time [37]. In the following years, other groups also confirmed both the low incidence of infection and the lack of statistical difference amongst those with and without diabetes mellitus [38 –42].

Sidi et al. reported their experience with penile prosthesis in patients with diabetes mellitus on immunosuppressive therapy following organ transplantation. They reported no infection or erosion with an average follow-up of 22.6 mo (range 6 mo to 5 y) [43].

Wilson et al. published their experience with the AMS InhibiZone coated penile prosthesis, reporting an infection rate of <1% in patients with diabetes mellitus, not substantially different from those without, in whom there were no infection (n = 467) [10].

The largest series to date was published by Eid et al. in 2012 reporting a reduction of device infection from 5.3% to 2% with the use of an infection-retardant-coated prosthesis in a mixed patient cohort. This rate was further reduced to 0.46% with the introduction of a “no touch” technique. The presence of diabetes mellitus did not influence the rate of infection [44].

Recently Chung et al. reported their outcomes over three decades with almost a thousand penile prostheses inserted with the most common implant being the AMS Ultrex (54%). Infection occurred in 0.8% with an equal incidence between patients with diabetes mellitus and pelvic trauma patients. There was no substantial difference in the prosthesis infection rate between men who received InhibiZone-coated and non-coated inflatable penile prosthesis with a mean follow-up of 76 (12–355) mo. The most important feature of this review was the low infection rate despite the high rate of revisions because of mechanical malfunction [45].

The most recently published case series from Song et al. in 2013 reviewed their experience with 201 penile prostheses. They implanted 45 malleable and 179 three-piece inflatable devices. Of the 201 patients, there was only one erosion and infection requiring prosthesis removal and whilst this was in a patient with diabetes mellitus, this was not a statistically significant finding [46].

Conclusions

It is clear that the most recent and largest series do not show any statistically significant increased infection rate in patients with diabetes mellitus [10,37 –46].

Older series reporting an increased infection rate amongst those with diabetes mellitus suffered from low patient numbers and a paucity of robust statistical analysis despite a greater rate of infection [24 –26]. The idea that patients with poorly controlled diabetes mellitus have a greater risk of infection, although perhaps logical, has not yet been proven and the only two studies that debate this date back to 1998 [9,28]. It is not correct to withhold the offer of a penile prosthesis to patients with poorly controlled diabetes mellitus on the grounds of a greater risk of infection as the evidence of this is poor. These patients should be consulted appropriately and undergo an extensive pre-operative work-up as the risk of intra and post-operative complications from other organ systems affected by diabetes mellitus are higher when their disease is not controlled leading to greater post-operative morbidity. Thus there exists strict criteria for diabetes mellitus control for elective surgery.

In the current era where expertise has developed so substantially as to render their reported infection rate as low as 0–1%, proves that other factors have a much greater impact on prosthesis infection than the presence of diabetes mellitus [38 –40,44,46 –48].

From this review we found the following factors contribute or prevent penile prosthesis infection:

1. Introduction of infection at the time of implantation can lead to a formation of bacterial biofilm in the implant spaces which prevents phagocytosis, impedes the diffusion of antibiotics and traps and concentrates nutrients for these bacteria [10,42,49]. This theory has been proven and it is rare that bacteria arrive in a lymphatic or hematogenous fashion.

2. Poor disinfection technique pre and intra-operatively can assist the inoculation of bacteria. Injury to the skin during shaving can increase infection risk and surgical scrubbing of the operative field and surgeons' hands are as mandatory as maintaining sterility with double gloving and changing of drapes before the implant is inserted [44,45].

3. Intra-operative antibiotic wash out of the area has proven to alter the outcomes of penile prostheses infection especially in revision cases [6,10,36,44,46]. Even though there is no standardized practice on the technique and type of solutions used these need to be adjusted to each patient and from the cultures grown from the prosthesis. In a time where new superbugs such as methicillin-resistant Staphylococcus aureus (MRSA), extended spectrum beta-lactamases (ESBL) and carbapenem-resistant enterobacteria are more noticeable and new antibiotics are implemented into practice, guidelines need to be reviewed frequently.

4. Infrequent placement of prostheses by a surgeon may lead to inexperienced operating room personnel and may increase the risk of inadvertent contamination of components and subsequently greater infection rates [50].

The formation of a bacterial biofilm is probably the most important factor facilitating infection in earlier case series. In penile prosthesis revision series, cultures from removed infected devices grew staphylococcus species with aureus and epidermis being the most common [42,49]. This is not surprising as microbiological research has found that Staphylococcus adheres to foreign surfaces with much greater affinity than other bacteria and then subsequently produces an exo-polysaccharide matrix preventing phagocytosis [49]. The effect of contamination of the surgical field during implantation is also evident from case series reporting a greater infection rate in patients with a history of urinary tract infections and neuropathic bladder [32]. These cases isolated enteric organisms and not staphylococcus species, with Escherichia coli being the most common [29,32,34].

It is clear from other branches of urology and surgery in general that outcomes relate to volume and this is also true of penile implant surgery with infection rates proven to be lower in high volume centers, although uninfluenced by the presence or otherwise of diabetes mellitus.

We acknowledged that most studies in this systematic review are case series and therefore of level 4 evidence. A national or preferably international dataset for penile prosthesis surgery and complications including patient demographic data and co-morbidity is essential to fully assess the impact of a variety of parameters and conditions of such surgery.

Footnotes

Acknowledgments

To the Edinburgh Surgical Sciences Qualification team for their support in this systematic review as part of an MSc at the University of Edinburgh.

Author Disclosure Statement

Ms. Christodoulidou and Mr. Pearce declare no conflict of interest and this study has not received any financial support from funding bodies.

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