Tropical Medicine and Infectious Disease Case Report Acute Hematogenous Periprosthetic Hip Infection by Gemella morbillorum, Successfully Treated with Debridement, Antibiotics and Implant Retention: A Case Report and Literature Review of Osteoarticular Gemella morbillorum Infections Albert Pardo-Pol 1, *, Daniel Pérez-Prieto 1 , Albert Alier 1 , Lucas Ilzarbe 2 , Lluïsa Sorlí 3 , Lluis Puig 1 , Santos Martínez-Díaz 1 and Joan Gómez-Junyent 3 1 Department of Orthopedics, Hospital del Mar, Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), Universitat Autònoma de Barcelona (UAB), CEXS-Universitat Pompeu Fabra, 08003 Barcelona, Spain 2 Department of Gastroenterology, Hospital del Mar, Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), Universitat Autònoma de Barcelona (UAB), CEXS-Universitat Pompeu Fabra, 08003 Barcelona, Spain 3 Department of Infectious Diseases, Hospital del Mar, Infectious Pathology and Antimicrobial Research Group (IPAR), Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), Universitat Autònoma de Barcelona (UAB), CEXS-Universitat Pompeu Fabra, 08003 Barcelona, Spain * Correspondence: apardoipol@psmar.cat Citation: Pardo-Pol, A.; Pérez-Prieto, Abstract: Gemella morbillorum is a facultative anaerobic, catalase-negative and non-spore forming D.; Alier, A.; Ilzarbe, L.; Sorlí, L.; Puig, Gram-positive cocci. It can be found as part of the normal oropharyngeal flora, in the gastrointestinal L.; Martínez-Díaz, S.; Gómez-Junyent, tract and the female genital tract. However, it can be a causal agent of infections such as endocarditis, J. Acute Hematogenous Periprosthetic Hip Infection by meningitis or brain abscesses, and very rarely can cause osteoarticular infections. Herein, a case Gemella morbillorum, Successfully report of an acute hematogenous prosthetic hip infection caused by Gemella morbillorum, successfully Treated with Debridement, treated with a DAIR and beta-lactam antibiotic therapy, is presented. We provide a literature review Antibiotics and Implant Retention: A of the other orthopedic-related infections caused by this microorganism. Case Report and Literature Review of Osteoarticular Gemella morbillorum Keywords: prosthetic joint infection; Gemella morbillorum; intestinal bacterial translocation; implant Infections. Trop. Med. Infect. Dis. 2022, retention 7, 191. https://doi.org/10.3390/ tropicalmed7080191 Academic Editor: John Frean 1. Introduction Received: 11 July 2022 Periprosthetic joint infection (PJI) is a serious complication that can occur after arthro- Accepted: 9 August 2022 plasty. It causes significant patient morbidity and poses a significant cost-burden for the Published: 18 August 2022 healthcare system. It occurs in 1 to 2% of primary arthroplasties, increasing to 4% in revision Publisher’s Note: MDPI stays neutral surgeries [1,2] with regard to jurisdictional claims in The prostheses can become infected in three ways. Infection can occur perioperatively, published maps and institutional affil- mostly through intraoperative inoculation, or after an hematogenous infection, occurring iations. at any time after implantation. It can also be the result of something more direct, such as spreading from a nearby infection e.g., adjacent osteomyelitis or soft tissue infection [3]. Gemella morbillorum (formerly known as Streptococcus morbillorum) is a facultative anaerobic, catalase-negative and non-spore forming Gram-positive cocci [4]. It can be found Copyright: © 2022 by the authors. as part of the normal oropharyngeal flora, in the gastrointestinal tract and the female genital Licensee MDPI, Basel, Switzerland. tract. However, it can be a causal agent of infections such as endocarditis, meningitis or This article is an open access article brain abscesses [5]. G. morbillorum was first described by Tunnicliff in 1917 [4]. Based on its distributed under the terms and biomolecular characteristics, it was included in the Gemella family in 1988. It has previously conditions of the Creative Commons Attribution (CC BY) license (https:// been denominated as Diplococcus morbillorum, Peptococcus morbillorum, Peptostreptococcus creativecommons.org/licenses/by/ morbillorum and Streptococcus morbillorum. Currently, there are four recognized species 4.0/). of Gemella spp.: G. haemolysans, G. morbillorum, G. sanguinis and G. bergeriae [6]. Dental Trop. Med. Infect. Dis. 2022, 7, 191. https://doi.org/10.3390/tropicalmed7080191 https://www.mdpi.com/journal/tropicalmed genital tract. However, it can be a causal agent of infections such as endocarditis, menin- gitis or brain abscesses [5]. G. morbillorum was first described by Tunnicliff in 1917 [4]. Based on its biomolecular characteristics, it was included in the Gemella family in 1988. It Trop. Med. Infect. Dis. 2022, 7, 191 has previously been denominated as Diplococcus morbillorum, Peptococcus morbillorum,2Pep- of 6 tostreptococcus morbillorum and Streptococcus morbillorum. Currently, there are four recog- nized species of Gemella spp.: G. haemolysans, G. morbillorum, G. sanguinis and G. bergeriae [6]. Dental procedures, gastrointestinal carcinomas [7], hepatorenal diseases, diabetes procedures, mellitus andgastrointestinal steroid therapycarcinomas [7], hepatorenal are predisposing diseases, in factors of infections diabetes humansmellitus [8,9]. and steroid therapy are predisposing factors of infections in humans [8,9]. Microbiological identification may be difficult, and the infection can go undetected. Microbiological identification may be difficult, and the infection can go undetected. Therefore, its true incidence has not been confirmed [10,11]. Streptococcus viridians may be Therefore, its true incidence has not been confirmed [10,11]. Streptococcus viridians may be misleading in microbiological studies because it also presents with alpha-hemolysis in the misleading in microbiological studies because it also presents with alpha-hemolysis in the blood agar. Sometimes, a polymerase chain reaction (PCR) may be needed for the proper blood agar. Sometimes, a polymerase chain reaction (PCR) may be needed for the proper identification of Gemella spp. infections, such as bacteremia, endocarditis or those affecting identification of Gemella spp. infections, such as bacteremia, endocarditis or those affecting the central nervous system [10–12]. the central nervous system [10–12]. Infections by G. morbillorum have been identified in all age groups and in both im- Infections by G. morbillorum have been identified in all age groups and in both im- munocompetent and immunosuppressed patients. However, anecdotal case reports of os- munocompetent and immunosuppressed patients. However, anecdotal case reports of teoarticular infections caused by G. morbillorum have been reported [13–19]. osteoarticular infections caused by G. morbillorum have been reported [13–19]. Herein, a case report of an acute hematogenous prosthetic hip infection caused by G. Herein, a case report of an acute hematogenous prosthetic hip infection caused by morbillorum G. morbillorum is is presented. presented.AAliterature literaturereview reviewof of the the other orthopedic-related infections other orthopedic-related infections caused by this microorganism is also provided. caused by this microorganism is also provided. 2. Case 2. Case Report Report This case involves This case involves aa 60-year-old 60-year-old woman woman with with aa history history ofof severe severe psoriasis psoriasis being being treatedwith treated withRisankizumab, Risankizumab,a humanized a humanized immunoglobulin immunoglobulin G1 G1 (IgG1) (IgG1) monoclonal monoclonal anti- antibody body selective selective to the to the interleukin interleukin (IL)-23(IL)-23 protein. protein. Her past Her past medical medicalhistory historyincluded includedobesity obesity(body (bodymass massindex index37 kg/m22), major depres- 37kg/m sive disorder sive disorder(MDD) (MDD)and and chronic chronicalcohol alcoholabuse. abuse. In In 2011, 2011, aa cemented cemented total total hip hip arthroplasty arthroplasty (THA)U2 (THA) U2prosthesis prosthesis (United (United Orthopedic Orthopedic Corporation, Corporation, NewNew Taipei, Taipei, Taiwan)Taiwan) was im- was implanted planted after the after woman theexperienced woman experienced a sub-capital a sub-capital fracture. fracture. In 2016, a In 2016, aprosthetic one-step one-step prosthetic exchange exchange was was performed performed due to stem due to stem loosening, loosening, for whichfor which a prosthesis a revision revision prosthesis (Zimmer(Zimmer Biomet, Biomet,Township, Wayne Wayne Township, IN, USA) IN, wasUSA) was implanted implanted (Figure(Figure 1). PJI1). wasPJIruled was ruled out based out based on on the IDSA’s 20132013 the IDSA’s criteria [20].[20]. criteria Figure 1. Figure 1. Hip Hip radiography radiography showing showing the the implanted implanted prosthesis. prosthesis. In February 2021, the patient came to the emergency department with acute pain in the operated hip, fever and erythema in the wound, which led us to suspect an acute periprosthetic infection. The blood test showed leukocytosis (10.2 × 109 /L) and an elevated level of C-reactive proteins (CRP: 153.6 mg/L). Arthrocentesis was performed and a PJI was diagnosed (231,000 cells/mm, of which 91% were neutrophils) according to the EBJIS criteria [21]. On the same day of admission, the patient underwent DAIR (debridement, antibiotics, irrigation and implant retention). A thorough debridement was performed to remove all periprosthetic infection. The blood test showed leukocytosis (10.2 × 109/L) and an elevated level of C-reactive proteins (CRP: 153.6 mg/L). Arthrocentesis was performed and a PJI was diagnosed (231,000 cells/mm, of which 91% were neutrophils) according to the EBJIS criteria [21]. Trop. Med. Infect. Dis. 2022, 7, 191 On the same day of admission, the patient underwent DAIR (debridement, antibiot- 3 of 6 ics, irrigation and implant retention). A thorough debridement was performed to remove all avascular and/or necrotic tissue. An exchange of the acetabular liner and the femoral head was performed. The removed components were sent for sonication, along with five avascular and/or necrotic tissue. An exchange of the acetabular liner and the femoral periprosthetic tissue samples for microbiological analysis. A histopathological analysis head was performed. The removed components were sent for sonication, along with five was requested for two samples. Non-alcoholic chlorhexidine irrigation with 9 liters was periprosthetic tissue samples for microbiological analysis. A histopathological analysis performed. was requestedThefor wound was closed, two samples. and incisional Non-alcoholic negative-pressure chlorhexidine therapy irrigation with (PICO) was 9 liters was carried out, along with two deep drains. Due to acute renal failure (GFR performed. The wound was closed, and incisional negative-pressure therapy (PICO) was 41 mL/min 1.73 m 2; 1.62 mg/dL creatinine), vancomycin was avoided and an empirical broad-spectrum carried out, along with two deep drains. Due to acute renal failure (GFR 41 mL/min 1.73 m2 ; antibiotic 1.62 mg/dL therapy with vancomycin creatinine), intravenouswas daptomycin avoided and850 an mg/daily empirical (10broad-spectrum mg/kg/day of antibi- actual body weight) and ceftazidime 2 g/12 h, administered by intermittent otic therapy with intravenous daptomycin 850 mg/daily (10 mg/kg/day of actual body infusion, was initi- ated. weight) and ceftazidime 2 g/12 h, administered by intermittent infusion, was initiated. The intraoperative The intraoperative tissue, tissue, synovial synovial fluid fluid and and sonication sonication fluid fluid cultures cultures were were positive positive for G. morbillorum (susceptible to penicillin and cefotaxime). After those results, for G. morbillorum (susceptible to penicillin and cefotaxime). After those results, antibiotic antibiotic therapy was therapy was modified modified to to entail entail the the intermittent intermittent infusion infusion ofof 22 g g cefotaxime cefotaxime every every 88 h,h, in in monotherapy. An monotherapy. An echocardiography echocardiographyshowed showedno novegetations vegetationsororother othersigns signsofofendocarditis. endocardi- tis. An An abdominal abdominal CT CTscanscan ruled ruled outout malignancy, malignancy, butbut thethe liver liver parenchyma parenchyma showed showed signs signs of of a previously undiagnosed chronic inflammation with moderate a previously undiagnosed chronic inflammation with moderate ascites (Figure 2). Theascites (Figure 2). The gastroscopyshowed gastroscopy showedsigns signsofofmild mildportal portalhypertension hypertension (without (without esophageal esophageal varices). varices). Dur- During ing the the colonoscopy, colonoscopy, a sessile a sessile adenoma adenoma waswas removed. removed. Thepatient The patientalso alsodenied deniedaa history history of procedures over dental procedures over the the past past few few months. months. inflammation of Figure 2. CT scan showing chronic inflammation of the the liver liver with with moderate moderate ascites. ascites. We We suspected suspected aa mixed mixed etiology etiology of of cirrhosis cirrhosis (a (a combination combination ofof heavy heavy alcohol alcohol intake intake and and nonalcoholic fatty liver disease). The laboratory results showed a GGT 411 U/L and nonalcoholic fatty liver disease). The laboratory results showed a GGT 411 U/L and ALP ALP 151 151 U/L, hypoalbuminemia (1.7 U/L, hypoalbuminemia (1.7 g/dL), an elevated g/dL), an elevated AST AST (54 (54 U/L) with normal U/L) with normal ALTALT (20 (20 U/L), cholesterol of U/L), cholesterol of9090mg/dL mg/dLand andTGTG6464mg/dL. mg/dL.The Thepatient patienthad a high had MCV a high MCV(111.3 fL) (111.3 and elevated gamma globulins (IgG 2308 mg/dL, IgA 1212 mg/dL and IgM fL) and elevated gamma globulins (IgG 2308 mg/dL, IgA 1212 mg/dL and IgM 202 mg/dL), 202 mg/dL), but with a negative autoimmunity study (ANA, AMA and SMA). HBV, HCV and HIV but with a negative autoimmunity study (ANA, AMA and SMA). HBV, HCV and HIV serologies were negative. serologies were negative. In conclusion, the patient was diagnosed with an acute hematogenous PJI after spon- taneous bacteremia due to gastrointestinal bacterial translocation, and in the context of decompensated cirrhosis (possibly of mixed etiology, due to excessive alcohol intake and nonalcoholic fatty liver disease). The liver pathology revealed significant alterations in coagulation and severe hy- poproteinemia (albumin levels 1.7–2 g/dL). These factors may have contributed to the persistent wound discharge. Due to this persistent drainage, despite the culture-negative swabs, a second DAIR was performed 10 days after the first surgery, with all cultures being negative in this case. At two weeks after the second intervention, the patient was discharged. Antibiotic therapy was modified to 1 g of oral amoxicillin every 8 h. Trop. Med. Infect. Dis. 2022, 7, 191 4 of 6 The patient went on to complete 3 months of uneventful antibiotic treatment. Although the patient was at risk of experiencing sporadic infections (due to her immunosuppressive treatments for psoriasis and cirrhosis), we consider the infection cured, so we decided not to use suppressive treatment. At the 18-month follow-up appointment, the patient was pain-free, with a Postel- Merle-d’Aubigné of 6-6-6 and a current BMI of 27 Kg/m2 . The liver cirrhosis is currently being monitored by hepatology and no further decompensation has presented. 3. Discussion We present a case of an acute hematogenous PJI caused by G. morbillorum that man- ifested with acute pain, functional impotence and fever. No prodromal symptoms were observed, as reported in other cases [18]. The infection was successfully treated with a DAIR and a second debridement after 10 days, which stands in contrast to the poor results described in the literature [22]. Osteoarticular infections due to G. morbillorum are rare (Table 1). Of all the reported cases, five were native septic arthritis [13,15], three of them were associated with an endovascular infection [16,18] or osteomyelitis [17], and two cases were associated with PJI (hip and elbow) [14,19]. To the best of our knowledge, the present case is the third case of PJI caused by G. morbillorum. Table 1. Summary of reported cases of septic joints caused by Gemella morbillorum. Predisposing Reference Sex, Age Joint Disease Surgery Antibiotic Therapy Factors Two-stage Von Essen et al., Total elbow Female, 45 Chronic fistula revision NS 1993 [19] arthroplasty arthroplasty Poor dentition. Bacteriemia. Omran and Male, 48 Wrist Possible infected Wrist aspiration Vancomycin 6 w Wood, 1993 [16] dialysis access graft Trochanter Van Dijk et al., osteomyelitis Chronic Open articular Penicillin G and clindamycin Male, 42 1999 [17] and ipsilateral corticoids lavage for 6 w. Oral clindamycin 3 w septic hip Czarnecki et al., Bacteriemia. Knee aspiration Male, 75 Knee Ceftriaxone 6 w 2007 [18] Endocarditis and irrigation Penicillin G and flucloxacillin Roche and Arthroscopic Male, 42 Knee NS 6 d. Oral amoxicillin and oral Smyth, 2005 [15] articular lavage flucloxacillin 5 flucloxacillin 5 w Cloxacillin and gentamicin 4 d. Two-stage Medina-Gens Total hip Cefotaxime and gentamicin Male, 41 Periodontitis revision et al., 2007 [14] arthroplasty 11 d. Penicillin G 22 d arthroplasty Teicoplanin and rifampicin Desmottes et al., Arthroscopic Amoxicillin/clavulanic acid. Female, 90 Knee Pseudogout 2018 [13] articular lavage Oral amoxicillin 6 w Daptomycin, cloxacillin and Present case, Total hip DAIR. Second ceftazidime 4 d. Cefotaxime and Female, 60 Cirrhosis 2021 arthroplasty DAIR after 10 d metronidazole 2 w Amoxicillin 4w The two previous cases of periprosthetic infections, both chronic infections, were treated with two-stage prosthetic replacement. We concluded that the management of this case of acute hematogenous infection with DAIR was an option supported by the literature. Trop. Med. Infect. Dis. 2022, 7, 191 5 of 6 According to the IDSA guidelines, patients should be considered for DAIR if the joint is less than 30 days old, or if the infectious symptoms last less than 21 days in the absence of a draining sinus tract [20]. Reported cases of septic arthritis in the native joint have been treated by means of arthroscopic lavage or aspiration and irrigation. As endocarditis is the most common infection associated with G. morbillorum, a careful cardiac examination is always performed to rule it out in the case of a positive blood culture for Gemella or an infection in another location. In this case, it was negative. Most of the reported cases involved predisposing or triggering factors of this infection. Those factors include endocarditis, gastrointestinal carcinoma, periodontitis and chronic corticosteroid use. This is the first case of osteoarticular infection caused by Gemella where the precipitating factor was advanced liver disease, specifically a previously undiagnosed decompensated cirrhosis due to alcoholic- and metabolic-associated fatty liver disease that was diagnosed after further study. This comorbidity conditioned the mechanism of the infection and the patient’s clinical course during admission. It is known that patients with liver cirrhosis have an increased risk of infection and in-hospital mortality or post- operative complications after surgery (renal, respiratory and infectious). Moreover, the hospitalization period and use of the intensive care unit are significantly greater among this population [19,20]. Intestinal bacterial translocation is a common cause of infections in cirrhotic patients, with the passage of viable bacteria or bacterial products from the intestinal lumen to the mesenteric lymph nodes and then to systemic circulation. This can lead to spontaneous bacterial peritonitis, which was ruled out in this case, or spontaneous bacteremia. In the case reported here, it turned out to be the latter, this being the final diagnosis proposed for this patient [23,24]. We used intravenous cefotaxime during hospital admission and oral amoxicillin for three months after hospital discharge. The isolated strain of Gram. Showed a susceptibility to all antibiotics: clindamycin (MIC ≤ 0.125 mg/L), cefotaxime (MIC ≤ 0.002 mg/L), peni- cillin (MIC ≤ 0.002 mg/L), vancomycin (MIC ≤ 0.25 mg/L) and rifampicin (MIC ≤ 0.002 mg/L). According to the literature, most cases of Gemella are susceptible to beta-lactams and van- comycin. Other antibiotics that may show activity against G. morbillorum are macrolides, levofloxacin and linezolid. They are inherently resistant to trimethoprim-sulfamethoxazole and streptomycin [25]. 4. Conclusions G. morbillorum osteoarticular infection is a rare but possibly underdiagnosed entity due to its difficult diagnosis. It should not be considered a contaminant if it is isolated in a synovial fluid analysis. We presented a case report of an acute hematogenous G. morbillorum infection successfully treated by means of DAIR and beta-lactam antibiotic therapy. Since most patients who experience this infection present with predisposing fac- tors, it is advisable to perform an echocardiography, gastroscopy, colonoscopy, and ab- dominopelvic CT scan, as well as an examination of the oropharynx and teeth, in order to identify an underlying condition. Spontaneous bacteremia of intestinal origin in patients with risk factors for immune dysfunction (e.g., liver cirrhosis) should also be considered in the differential diagnosis. Author Contributions: Conceptualization: A.P.-P.; methodology A.P.-P.; formal analysis and investi- gation A.P.-P.; writing-origial draft preparation A.P.-P., D.P.-P. and J.G.-J.; writing-review and editing A.P.-P., D.P.-P., L.I., L.S. and J.G.-J.; Supervision: A.A., S.M.-D. and L.P. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: The study did not require ethical approval. The study was conducted in accordance with de Declaration of Helsinki. Informed Consent Statement: Informed consent was obtained from all subjects involved in the study. Trop. Med. Infect. Dis. 2022, 7, 191 6 of 6 Data Availability Statement: The datasets used in the current study are available from the corre- sponding author on reasonable request. Conflicts of Interest: The authors declare no conflict of interest. References 1. Hosny, H.A.; Keenan, J. Management of prosthetic joint infection. 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