Skip to main content

Maternal septicemia caused by Streptococcus mitis: a possible link between intra-amniotic infection and periodontitis. Case report and literature review

Abstract

Background

Intra-amniotic infection has a strong causal association with spontaneous preterm birth and preterm prelabor rupture of membranes (PPROM). The most common route of intra-amniotic infection is the ascending pathway in which microorganisms from the vagina gain access to the amniotic cavity. Distant microorganisms such as those from the oral cavity have been reported in intra-amniotic infection through hematogenous spreading.

Case presentation

A 31-year-old gravida 1, para 0 Thai woman at 33+6 weeks’ gestation presented with leakage of vaginal fluid and irregular uterine contraction. She developed fever at 4 h after admission and was later diagnosed with acute chorioamnionitis. A Cesarean section was performed to terminate pregnancy. In addition to a blood culture, the cultures of amniotic fluid, vaginal and chorioamniotic membrane swabs were positive for Streptococcus mitis with identical susceptibility profiles. After the delivery and antibiotic prescription, oral examination showed dental caries and chronic periodontitis.

Conclusions

This is the first case report demonstrating maternal septicemia and intra-amniotic infection caused by S. mitis which might be attributed to periodontitis in women presenting with preterm PROM. We highlighted the association of periodontal disease and preterm labor/PROM syndrome. Oral cavity examination should be included in the prenatal care to ensure good dental hygiene.

Peer Review reports

Background

Intra-amniotic infection and/or inflammation is causally linked with spontaneous preterm birth and preterm prelabor rupture of membranes (PPROM) [1, 2]. The frequencies of intra-amniotic infection/inflammation in preterm labor and PPROM are approximately 30% and 50%, respectively [1,2,3,4,5,6,7]. While an ascending migration from the vagina is preponderant, pathogens may also gain access to the amniotic cavity by other pathways such as hematogenous dissemination or accidental introduction at the time of an invasive prenatal procedure [1, 2, 8,9,10,11,12,13,14]. Bearfield et al. identified similar strains of Fusobacterium nucleotum (F. nucleotum) and Streptococcus spp. from dental plaque and amniotic fluid, which suggests an oral origin of amniotic fluid microorganism infection [15]. Subsequently, other oral bacteria such as Capnocytophaga spp., Rothia dentocariosa and Eikenella corodens have also been detected in amniotic fluid [15,16,17,18,19,20,21,22,23,24].

Streptococcus mitis (S. mitis), a member of viridans streptococci, is prevalent in the normal flora in the oropharynx [25, 26]. There have thus far been two case reports of acute histological chorioamnionitis caused by S. mitis [27, 28]. Both studies showed that S. mitis was identified in placental culture. Antecedent cunnilingus and dental scaling are proposed to be associated with S. mitis infection [28]. One report described that S. mitis is one of the polymicrobial microorganisms detected in the mid-trimester amniotic fluid of women who subsequently had fetal death [29].

Herein, we reported a unique case of S. mitis septicemia in a woman presenting with PPROM and clinical chorioamnionitis. Samples of amniotic fluid, vagina, chorioamniotic membranes, and maternal blood were taken for aerobic cultures. The results demonstrated similar strains of S. mitis. The patient was subsequently confirmed to have deep dental caries and chronic periodontitis. This is the first case report demonstrating septicemia, clinical chorioamnionitis and intra-amniotic infection may be presumably due to chronic periodontitis.

Case presentation

A 31-year-old gravida 1, para 0 Thai woman at 33 weeks and 6 days of gestation presented at the labor and delivery unit due to the leakage of amniotic fluid at 26 h prior to the admission. Her antenatal care was unremarkable except for morbid obesity (body mass index 44.5 kg/m2) and pre-gestational diabetes. She was administered 81 mg of aspirin and 16 units of insulin daily. Her fasting and two-hour postprandial blood sugar ranged between 106–123 and 99–131 mg/dL, respectively. Her blood test, serology and ultrasound abnormality examination were normal. She had no underlying disease and denied a history of smoking, alcoholic drinking, or illicit drug use.

At 33+6 weeks’ gestation, she complained of vaginal leaking fluid and irregular uterine contraction 26 h prior to the admission. She had no fever or vaginal bleeding. Her fetal movement was good. Her vital signs showed no abnormalities. A dry sterile speculum examination revealed clear pooling fluid in the vagina with positive cough and nitrazine tests. Vaginal examination showed the cervix was 2 cm dilated with the effacement of 25%. Her white blood cell count (WBC) was 13,450 cells/mm3 with 80% neutrophil. Urinalysis was normal. External fetal monitoring demonstrated normal fetal heart rate and variability. Transabdominal ultrasonography examination demonstrated that the fetal growth was normal; however, the amniotic fluid index was only 2 cm. Therefore, we did not perform any amniocentesis for the determination of intra-amniotic infection/inflammation status. Expectant management was performed; steroid as well as antibiotic therapy (intravenous ampicillin, azithromycin) were given to promote lung maturity and prolong latency period, respectively.

The patient developed fever (38.2 °C) around 4 h after admission. Her pulse and blood pressure were 90 bpm and 121/71 mmHg, respectively. Continuous cardiotocography demonstrated a fetal heart rate of 165 bpm with moderate variability. Uterine contractions were 3-min intervals with moderate intensity. No uterine tenderness or foul-smelling discharge was found. Her WBC and C-reactive protein (CRP) were elevated (WBC 17,940 cells/mm3 with 85.4% neutrophil, CRP 24.36 mg/dL). Clinical chorioamnionitis was diagnosed and oxytocin was given to augment labor progression. The antibiotics were changed to intravenous ceftriaxone (2 g/every 24 h), intravenous metronidazole (500 mg/every 8 h), and oral clarithromycin (500 mg/every 8 h) to treat intra-amniotic infection as recommended in previous studies [30,31,32,33]. Her cervical progression was arrested at 4 cm for 4 h; hence, Cesarean delivery was performed. She delivered a male fetus with Apgar score of 8, 10 at 1 min and 5 min after delivery, respectively. Birth weight of the baby was 2680 g.

After delivery, she received similar antibiotics. Cultivation of blood culture (taken at the time of fever), amniotic fluid obtained during Cesarean delivery, vaginal swab (obtained at the time of hospital admission) and placental swab (chorioamniotic membranes) revealed bacterial colonies identified as S. mitis (Fig. 1). Gram stain from enriched hemoculture showed Gram positive cocci in chains (Fig. 2). Interestingly, antibiotic sensitivity profiles from all specimens were similar (Table 1). Since her male neonate had respiratory distress, and severe hypoglycemia (blood sugar 16 mg/dL), which could be the sign of early onset neonatal sepsis, he was diagnosed with presumed sepsis requiring treatment. The diagnosis of presumed sepsis was based on intrapartum risk factor which involves the presence of intra-amniotic infection and the presence of respiratory distress as well as severe hypoglycemia requiring treatment in neonate [34]. Although, his WBC count, hemoculture and chest x-ray were within normal limits, infection could be present in the newborn. CRP value could be in normal limit due to low CRP value in preterm newborns. Therefore, he was given intravenous ampicillin and gentamicin for 7 days which is based on the recommendation by the American Academy of Pediatrics and the Centers for Disease Control and Prevention (CDC) [35, 36].

Fig. 1
figure 1

Blood agar plate showing colonies obtained from: a peripheral blood; b vaginal swab; c amniotic fluid and; d placenta

Fig. 2
figure 2

Gram stain from hemoculture showing gram-positive cocci in chain

Table 1 Antibiotics sensitivity profile of the organisms derived from maternal blood, amniotic fluid, vaginal and placental cultures

Since the patient was diagnosed with septicemia and S. mitis is usually found in the oral cavity, we consulted a dentist and an infectious consultant to determine the source of infection. Dental examination showed multiple dental caries with nearly exposed pulp, pulp necrosis and acute apical periodontitis (Fig. 3). Tooth extraction and curettage were performed. Vancomycin was intravenously administered for 1 week according to antibiotic sensitivity profile. At 6th week postpartum, her vaginal and dental caries bacterial culture demonstrated no S. mitis, and her clinical course was unremarkable. Placental histopathological examination confirmed acute histological chorioamnionitis stage 1 grade 2 (Fig. 4A and B). Gram positive cocci in chains was identified at chorioamniotic membranes. Retrospectively, the patient denied oral sexual intercourse during pregnancy. She reported that she subjectively had dental caries 1 year ago but did not get the treatment. The last time that she saw the dentist was more than 10 years. She did not receive dental treatment during this pregnancy. “Her partner denied having periodontal disease; however, he did not have a clinical assessment performed to determine periodontal disease status.”

Fig. 3
figure 3

A Pulp necrosis with acute apical periodontitis, deep dental carries; B Dental X-ray: Fracture right lower molar tooth

Fig. 4
figure 4

Pathology of chorioamnionitis: A Gross specimen of the placenta. Round shape of fresh placenta size 18.5 × 17 × 3 cm at fetal surface, shows turbid membranes. The tan umbilical cord inserts at central area; B Histopathology of chorioamniotic membranes. The membranes show acute chorioamnionitis stage 1 grade 2. Confluence of neutrophils infiltrates in the chorion or subchorionic space; * demonstrates neutrophils (H&E stain × 20). The Olympus BX53 microscope attached with Olympus DP73 digital camera and cellSens dimension software was used for microscopic study and photography

Discussion and conclusions

We reported a unique case with intra-amniotic infection, clinical chorioamnionitis and septicemia from S. mitis in a woman presenting with PPROM. Interestingly, the profiles of antibiotic sensitivity are identical among bacteria derived from amniotic fluid, vagina, chorioamniotic membranes and maternal blood, which suggests a similar bacterial strain. Multiple tooth decay and periodontitis were subsequently revealed. These observations suggested a link between periodontal disease and intra-amniotic infection. This is the first case report demonstrating maternal septicemia and intra-amniotic infection caused by S. mitis associated with periodontitis in the women presenting with PROM.

Periodontal disease is defined as a wide range of chronic inflammatory conditions of the gingiva (also called gums, the soft tissue surrounding the teeth), bone and ligament (the connective tissue collagen fibers anchoring the tooth to alveolar bone) that altogether support the teeth [37,38,39]. The initial stage usually begins with localized inflammation of the gingiva or “gingivitis” caused by bacteria in the dental plaque, a biofilm of microorganisms observed in the tooth surface [37,38,39,40]. Subsequently, untreated gingivitis leads to “chronic periodontitis” affecting surrounding epithelial tissues, the gingiva, alveolar bone and periodontal ligament, and eventually leads to tooth loss [37,38,39].

Accumulating evidence has shown that there is a relationship between periodontal disease and spontaneous preterm labor. The latest systematic review and meta-analysis including 16 case–control and 4 cohort studies demonstrated that periodontitis increases the risk of preterm birth about twofold (odd ratios 2.01; 95%; confidence interval 1.71–2.36) [41]. However, the definition of periodontitis is inconsistent among these studies [41]. Proposed mechanisms whereby periodontitis is associated with preterm labor are thought to be related to systemic inflammation [34, 39,40,41]. Oral pathogens could enter the maternal bloodstream and amniotic cavity causing inflammatory cascade in the fetoplacental unit triggering a common pathway of preterm labor [1, 2, 12, 42,43,44]. In animal studies, intravenous injection of F. nucleatum into pregnant mice resulted in premature delivery and stillbirths [42]. F. nucleatum colonizes in the uterus, amniotic fluid, and the placenta through hematogenous route [23]. In addition, oral pathogens such as Streptoccoccus spp., F. nucleatum, Eikenella corodens, and Capnocytophaga species are detected in the amniotic fluid of women with preterm labor or second trimester abortion [15,16,17,18,19,20,21,22,23,24]. In addition, dysbiosis of the placental microbiome has been reported to be associated with preterm birth [43,44,45,46,47,48,49]. Aagaard et al. characterized the placental microbiome using the metagenomic data derived from 16S rDNA as well as the whole genome sequencing and demonstrated that the placenta has a low abundance of microbiome composed of nonpathogenic commensal microbiota from the Proteobacteria, Tenericutes, Firmicutes, Bacteroidetes and Fusobacteria phyla. Importantly, such placental microbiome was shown to be most similar to the oral microbiome, and it is also associated with preterm birth [43]. Subsequently, several studies have determined placental microbiome dysbiosis in women with preterm birth [43,44,45,46,47,48,49,50,51,52,53,54,55]. However, it is still unclear whether periodontal therapy can reduce the frequency of preterm labor [46, 47].

Streptococcus mitis was first isolated and discovered by Andrews and Horder in 1986 from the human oropharynx [56]. The genus name ‘mitis’, based on the Latin root ‘mitis’, means “mild”, indicating low pathogenicity and virulence involved in different types of mild infections [26]. This species is a predominant pioneer colonizer of the oral cavity after birth and persists through life [57]. It also colonizes in other areas of the human body such as the skin, and the gastrointestinal and genital tracts as a part of the normal flora [26] although its presence in the vaginal flora is rare (2%) [58]. In the oropharynx, S. mitis is thought to form oral biofilms by supplying adherence sites for secondary colonizers [26, 59]. This bacterium can cause a variety of infectious complications including bacterial infective endocarditis, bacteremia, septicemia, meningitis, eye infections, and pneumonia, especially in elderly patients or immunocompromised patients [25, 28]. Currently, mortality rate from S. mitis bacteremia has not been reported. Nevertheless, mortality rates from viridans Streptococcus bacteremia range from 6 to 30% in immunocompromised hosts [60]. S. mitis colonizes the human oropharynx by several mechanisms including the expression of adhesins, production of immunoglobulin A proteases, and modulation of the host immune response [25, 26, 28]. Moreover, comparative genomic analysis confirms the presence of virulence genes such as hyaluronic acid synthesis-associated genes, which promote colonization and prevent bacteria from phagocytosis [61]. Importantly, bacteremia (including S. mitis) can occur after tooth brushing or other dental procedures [62,63,64,65]. The number of S. mitis significantly increases during pregnancy and is associated with dental caries, especially during the second and third trimester [66]. S. mitis has been infrequently isolated in the amniotic fluid of women with preterm labor (1.8%) [3, 5, 6], PPROM (2–3%) [4, 7] or short cervix (0.4%) [67].

Two previous reports discussed S. mitis in women with preterm labor and chorioamnionitis [27, 28]. Schmiedel et al. reported that S. mitis was identified from placental and fetal membranes by cultivation, fluorescence in situ hybridization and DNA sequencing techniques in women with clinical chorioamnionitis [27]. In this study, S. mitis could be identified only in the superficial layers of the fetal membranes but was found to be absent in the placental tissue, thereby indicative of ascending infection. However, there were no results of vaginal, blood or amniotic fluid microbiological examination. In addition, the source of S. mitis was not evaluated. A recent report by Hosseini et al. showed that S. mitis was isolated from amniotic membrane cultivation in a pregnant woman presenting with preterm labor at 21+5 weeks’ gestation who had no evidence of clinical chorioamnionitis [28]. The patient had a history of dental scaling and cunnilingus with her husband who had periodontal disease about 2 weeks prior to the onset of preterm labor. The authors hypothesize that acute histological chorioamnionitis caused by S. mitis is attributable to dental scaling or cunnilingus. However, this case was not confirmed to have periodontal disease or intra-amniotic infection since no amniotic fluid culture was performed. Even though one study demonstrated that S. mitis could be transmitted from a male partner to a female partner via vaginal intercourse, the mechanism has remained unclear [68]. S. mitis was also identified as one of the polymicrobial microorganisms detected in mid-trimester amniocentesis in asymptomatic pregnant women who subsequently experienced fetal death at 18 weeks’ gestation [29]. Other reports have shown evidence of intra-amniotic infection by viridans Streptococci and S. mutans in women presenting with preterm labor or short cervix [17, 18, 20, 22]. Interestingly, a successful eradication of such microorganisms is possible [17, 18, 22]. Table 2 described previous reports of S. mitis in acute chorioamnionitis cases.

Table 2 Reported cases of acute clinical chorioamnionitis caused by Streptococcus mitis

In conclusion, we reported a PPROM case with intra-amniotic infection and septicemia caused by S. mitis. This particular pathogen was systematically isolated from the samples of amniotic fluid, maternal blood, vaginal and chorioamniotic membranes with similar antibiotic sensitivity profiles indicating a similar strain. Subsequently, multiple dental caries and chronic periodontitis were identified and thought to be the possible source. Although the identification of S. mitis in dental plaque had not been performed in our case as we already initiated antibiotic therapy, it is possible that periodontitis found in the patient could have led to a bacteremia and septicemia resulting in intra-amniotic infection and PPROM. Altogether, these observations support the hypothesis that oral bacteria can gain access into the amniotic cavity through hematogenous dissemination [43, 49]. Therefore, prenatal care should include oral cavity examination to ensure good dental hygiene [69,70,71,72]. If possible, dental care should be performed prior to pregnancy to prevent maternal septicemia or other associated infections caused by oral bacteria and to maintain overall health of pregnant woman.

We reported a case with intra-amniotic infection, clinical chorioamnionitis and septicemia caused by S. mitis. Dental caries or chronic periodontitis may be a source of intra-amniotic infection, thereby highlighting an association of periodontal disease and preterm labor/PROM syndrome. This is the first case report demonstrating S. mitis septicemia and clinical chorioamnionitis that develops from chronic periodontitis and tooth decay. We, here, support proper dental hygiene [72] and promote dental care, including identification, prevention and treatment of oral diseases, before and during pregnancy.

Availability of data and materials

All data generated or analyzed during this study are included in this published article [and the additional information files].

Abbreviations

CRP:

C-reactive protein

PROM:

Prelabor rupture of membranes

PPROM:

Preterm prelabor rupture of membranes

WBC:

White blood cell

References

  1. Romero R, Espinoza J, Kusanovic JP, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M. The preterm parturition syndrome. BJOG. 2006;113(Suppl 3):17–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science. 2014;345(6198):760–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, Erez O, Edwin S, Relman DA. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS ONE. 2008;3(8): e3056.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. DiGiulio DB, Romero R, Kusanovic JP, Gómez R, Kim CJ, Seok KS, Gotsch F, Mazaki-Tovi S, Vaisbuch E, Sanders K, et al. Prevalence and diversity of microbes in the amniotic fluid, the fetal inflammatory response, and pregnancy outcome in women with preterm pre-labor rupture of membranes. Am J Reprod Immunol. 2010;64(1):38–57.

    PubMed  PubMed Central  Google Scholar 

  5. Romero R, Miranda J, Chaiworapongsa T, Chaemsaithong P, Gotsch F, Dong Z, Ahmed AI, Yoon BH, Hassan SS, Kim CJ, et al. A novel molecular microbiologic technique for the rapid diagnosis of microbial invasion of the amniotic cavity and intra-amniotic infection in preterm labor with intact membranes. Am J Reprod Immunol. 2014;71(4):330–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Romero R, Miranda J, Chaiworapongsa T, Korzeniewski SJ, Chaemsaithong P, Gotsch F, Dong Z, Ahmed AI, Yoon BH, Hassan SS, et al. Prevalence and clinical significance of sterile intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Reprod Immunol. 2014;72(5):458–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Romero R, Miranda J, Chaemsaithong P, Chaiworapongsa T, Kusanovic JP, Dong Z, Ahmed AI, Shaman M, Lannaman K, Yoon BH, et al. Sterile and microbial-associated intra-amniotic inflammation in preterm prelabor rupture of membranes. J Matern Fetal Neonatal Med. 2015;28(12):1394–409.

    Article  PubMed  CAS  Google Scholar 

  8. Benirschke K, Clifford SH. Intrauterine bacterial infection of the newborn infant: frozen sections of the cord as an aid to early detection. J Pediatr. 1959;54(1):11–8.

    Article  CAS  PubMed  Google Scholar 

  9. Blanc WA. Pathways of fetal and early neonatal infection. Viral placentitis, bacterial and fungal chorioamnionitis. J Pediatr. 1961;59:473–96.

    Article  CAS  PubMed  Google Scholar 

  10. Riscoll SG. Pathology and the developing fetus. Pediatr Clin North Am. 1965;12:493–514.

    Article  CAS  PubMed  Google Scholar 

  11. Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R, Sabo V, Athanassiadis AP, Hobbins JC. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol. 1989;161(3):817–24.

    Article  CAS  PubMed  Google Scholar 

  12. Romero R, Espinoza J, Gonçalves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med. 2006;11(5):317–26.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Romero R, Espinoza J, Gonçalves LF, Kusanovic JP, Friel L, Hassan S. The role of inflammation and infection in preterm birth. Semin Reprod Med. 2007;25(1):21–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Romero R, Gotsch F, Pineles B, Kusanovic JP. Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr Rev. 2007;65(12 Pt 2):S194-202.

    Article  PubMed  Google Scholar 

  15. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG. 2002;109(5):527–33.

    Article  PubMed  Google Scholar 

  16. McDonald H, Gordon DL. Capnocytophaga species: a cause of amniotic fluid infection and preterm labour. Pathology. 1988;20(1):74–6.

    Article  CAS  PubMed  Google Scholar 

  17. Mazor M, Chaim W, Hershkowitz R, Wiznitzer A. Eradication of Viridans streptococci from the amniotic cavity with transplacental antibiotic treatment. Arch Gynecol Obstet. 1994;255(3):147–51.

    Article  CAS  PubMed  Google Scholar 

  18. Mazor M, Chaim W, Meirovitz M, Yohay D, Leiberman JR, Glezerman M. Eradication of viridans streptococci from the amniotic cavity by parenteral antibiotic administration. A case report. J Reprod Med. 1995;40(11):820–2.

    CAS  PubMed  Google Scholar 

  19. Alanen A, Laurikainen E. Second-trimester abortion caused by Capnocytophaga sputigena: case report. Am J Perinatol. 1999;16(4):181–3.

    Article  CAS  PubMed  Google Scholar 

  20. Gherman RB, Browning J, Tramont J, Eggleston MK. Streptococcus viridans intra-amniotic infection associated with antecedent cunnilingus. Aust N Z J Obstet Gynaecol. 1999;39(2):257–9.

    Article  CAS  PubMed  Google Scholar 

  21. Kostadinov S, Pinar H. Amniotic fluid infection syndrome and neonatal mortality caused by Eikenella corrodens. Pediatr Dev Pathol. 2005;8(4):489–92.

    Article  PubMed  Google Scholar 

  22. Morency AM, Rallu F, Laferrière C, Bujold E. Eradication of intra-amniotic Streptococcus mutans in a woman with a short cervix. J Obstet Gynaecol Can. 2006;28(10):898–902.

    Article  PubMed  Google Scholar 

  23. Gauthier S, Tétu A, Himaya E, Morand M, Chandad F, Rallu F, Bujold E. The origin of Fusobacterium nucleatum involved in intra-amniotic infection and preterm birth. J Matern Fetal Neonatal Med. 2011;24(11):1329–32.

    Article  CAS  PubMed  Google Scholar 

  24. Bohrer JC, Kamemoto LE, Almeida PG, Ogasawara KK. Acute chorioamnionitis at term caused by the oral pathogen Fusobacterium nucleatum. Hawaii J Med Public Health. 2012;71(10):280–1.

    PubMed  PubMed Central  Google Scholar 

  25. Patterson MJ. Streptococcus. In: Baron S, editor. Medical microbiology. Galveston (TX): University of Texas Medical Branch; 1996.

    Google Scholar 

  26. Mitchell J. Streptococcus mitis: walking the line between commensalism and pathogenesis. Mol Oral Microbiol. 2011;26(2):89–98.

    Article  CAS  PubMed  Google Scholar 

  27. Schmiedel D, Kikhney J, Masseck J, Rojas Mencias PD, Schulze J, Petrich A, Thomas A, Henrich W, Moter A. Fluorescence in situ hybridization for identification of microorganisms in acute chorioamnionitis. Clin Microbiol Infect. 2014;20(9):O538-541.

    Article  CAS  PubMed  Google Scholar 

  28. Hosseini BS, Hunt J. Streptococcus mitis Chorioamnionitis after dental scaling and oral sex. Case Rep Obstet Gynecol. 2020;2020:9251731.

    PubMed  PubMed Central  Google Scholar 

  29. Waites KB, Bobo RA, Davis RO, Brookings ES, Cassell GH. Clinically silent polymicrobial amnionitis and intrauterine fetal death associated with a Cu-7 intrauterine contraceptive device. Am J Obstet Gynecol. 1984;150(8):998–9.

    Article  CAS  PubMed  Google Scholar 

  30. Lee J, Romero R, Kim SM, Chaemsaithong P, Park CW, Park JS, Jun JK, Yoon BH. A new anti-microbial combination prolongs the latency period, reduces acute histologic chorioamnionitis as well as funisitis, and improves neonatal outcomes in preterm PROM. J Matern Fetal Neonatal Med. 2016;29(5):707–20.

    Article  PubMed  Google Scholar 

  31. Lee J, Romero R, Kim SM, Chaemsaithong P, Yoon BH. A new antibiotic regimen treats and prevents intra-amniotic inflammation/infection in patients with preterm PROM. J Matern Fetal Neonatal Med. 2016;29(17):2727–37.

    CAS  PubMed  Google Scholar 

  32. Yoon BH, Romero R, Park JY, Oh KJ, Lee J, Conde-Agudelo A, Hong JS. Antibiotic administration can eradicate intra-amniotic infection or intra-amniotic inflammation in a subset of patients with preterm labor and intact membranes. Am J Obstet Gynecol. 2019;221(2):142.e141-142.e122.

    Article  CAS  Google Scholar 

  33. Yeo L, Romero R, Chaiworapongsa T, Para R, Johnson J, Kmak D, Jung E, Yoon BH, Hsu CD. Resolution of acute cervical insufficiency after antibiotics in a case with amniotic fluid sludge. J Matern Fetal Neonatal Med. 2021. https://doi.org/10.1080/14767058.2021.1881477.

    Article  PubMed  Google Scholar 

  34. Wirtschafter DD, Padilla G, Suh O, Wan K, Trupp D, Fayard EE. Antibiotic use for presumed neonatally acquired infections far exceeds that for central line-associated blood stream infections: an exploratory critique. J Perinatol. 2011;31(8):514–8.

    Article  CAS  PubMed  Google Scholar 

  35. Polin RaR, T. M.: Perinatal infections and chorioamnionitis. In: Martin RJF, A. A.; Walsh, M. C Ed. Fanaroff and Martin's neonatal-perinatal medicine. Volume 1, 11 edn. Elsevier; 2020: 404–414.

  36. Esper F: Postnatal bacterial infections. In: Martin RJF, A. A.; Walsh, M. C Eds. Fanaroff and Martin's neonatal-perinatal medicine. Volume 1, 11 edn. Elsevier; 2020: 789–808.

  37. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366(9499):1809–20.

    Article  PubMed  Google Scholar 

  38. Kinane DF, Stathopoulou PG, Papapanou PN. Periodontal diseases. Nat Rev Dis Primers. 2017;3:17038.

    Article  PubMed  Google Scholar 

  39. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Clin Periodontol. 2018;45(Suppl 20):S162-s170.

    Article  PubMed  Google Scholar 

  40. Marsh PD. Dental plaque as a biofilm and a microbial community—implications for health and disease. BMC Oral Health. 2006;6(Suppl 1):S14.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Manrique-Corredor EJ, Orozco-Beltran D, Lopez-Pineda A, Quesada JA, Gil-Guillen VF, Carratala-Munuera C. Maternal periodontitis and preterm birth: systematic review and meta-analysis. Community Dent Oral Epidemiol. 2019;47(3):243–51.

    Article  PubMed  Google Scholar 

  42. Han YW, Redline RW, Li M, Yin L, Hill GB, McCormick TS. Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun. 2004;72(4):2272–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra265.

    Article  CAS  Google Scholar 

  44. Doyle RM, Alber DG, Jones HE, Harris K, Fitzgerald F, Peebles D, Klein N. Term and preterm labour are associated with distinct microbial community structures in placental membranes which are independent of mode of delivery. Placenta. 2014;35(12):1099–101.

    Article  CAS  PubMed  Google Scholar 

  45. Antony KM, Ma J, Mitchell KB, Racusin DA, Versalovic J, Aagaard K. The preterm placental microbiome varies in association with excess maternal gestational weight gain. Am J Obstet Gynecol. 2015;212(5):653.e651-616.

    Article  Google Scholar 

  46. Prince AL, Ma J, Kannan PS, Alvarez M, Gisslen T, Harris RA, Sweeney EL, Knox CL, Lambers DS, Jobe AH, et al. The placental membrane microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. Am J Obstet Gynecol. 2016;214(5):627.e621-627.e616.

    Article  Google Scholar 

  47. Leon LJ, Doyle R, Diez-Benavente E, Clark TG, Klein N, Stanier P, Moore GE. Enrichment of clinically relevant organisms in spontaneous preterm-delivered placentas and reagent contamination across all clinical groups in a large pregnancy cohort in the United Kingdom. Appl Environ Microbiol. 2018;84(14):e00483.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Chu DM, Seferovic M, Pace RM, Aagaard KM. The microbiome in preterm birth. Best Pract Res Clin Obstet Gynaecol. 2018;52:103–13.

    Article  PubMed  Google Scholar 

  49. Prince AL, Chu DM, Seferovic MD, Antony KM, Ma J, Aagaard KM. The perinatal microbiome and pregnancy: moving beyond the vaginal microbiome. Cold Spring Harb Perspect Med. 2015;5(6):a023051.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Farooqi HMU, Kim KH, Kausar F, Muhammad J, Bukhari H, Choi KH. Frequency and molecular characterization of Staphylococcus aureus from placenta of mothers with term and preterm deliveries. Life. 2022;12(2):257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Seferovic MD, Pace RM, Carroll M, Belfort B, Major AM, Chu DM, Racusin DA, Castro ECC, Muldrew KL, Versalovic J, et al. Visualization of microbes by 16S in situ hybridization in term and preterm placentas without intraamniotic infection. Am J Obstet Gynecol. 2019;221(2):146.e141-146.e123.

    Article  CAS  Google Scholar 

  52. Fischer LA, Demerath E, Bittner-Eddy P, Costalonga M. Placental colonization with periodontal pathogens: the potential missing link. Am J Obstet Gynecol. 2019;221(5):383-392.e383.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Brummaier T, Syed Ahamed Kabeer B, Lindow S, Konje JC, Pukrittayaamee S, Utzinger J, Toufiq M, Antoniou A, Marr AK, Suriyakan S, et al. A prospective cohort for the investigation of alteration in temporal transcriptional and microbiome trajectories preceding preterm birth: a study protocol. BMJ Open. 2019;9(1):e023417.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Leiby JS, McCormick K, Sherrill-Mix S, Clarke EL, Kessler LR, Taylor LJ, Hofstaedter CE, Roche AM, Mattei LM, Bittinger K, et al. Lack of detection of a human placenta microbiome in samples from preterm and term deliveries. Microbiome. 2018;6(1):196.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Doyle RM, Harris K, Kamiza S, Harjunmaa U, Ashorn U, Nkhoma M, Dewey KG, Maleta K, Ashorn P, Klein N. Bacterial communities found in placental tissues are associated with severe chorioamnionitis and adverse birth outcomes. PLoS ONE. 2017;12(7): e0180167.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Kilian M, Mikkelsen L, Henrichsen J. Taxonomic Study of Viridans Streptococci: description of Streptococcus gordonii sp. Nov. and emended descriptions of Streptococcus sanguis (White and Niven 1946), Streptococcus oralis (Bridge and Sneath 1982), and Streptococcus mitis (Andrewes and Horder 1906). Int J Syst Evolut Microbiol. 1989;39:471–84.

    Google Scholar 

  57. Pearce C, Bowden GH, Evans M, Fitzsimmons SP, Johnson J, Sheridan MJ, Wientzen R, Cole MF. Identification of pioneer viridans streptococci in the oral cavity of human neonates. J Med Microbiol. 1995;42(1):67–72.

    Article  CAS  PubMed  Google Scholar 

  58. Rabe LK, Winterscheid KK, Hillier SL. Association of viridans group streptococci from pregnant women with bacterial vaginosis and upper genital tract infection. J Clin Microbiol. 1988;26(6):1156–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Kolenbrander PE, London J. Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol. 1993;175(11):3247–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Bochud PY, Calandra T, Francioli P. Bacteremia due to viridans streptococci in neutropenic patients: a review. Am J Med. 1994;97(3):256–64.

    Article  CAS  PubMed  Google Scholar 

  61. Zheng W, Tan TK, Paterson IC, Mutha NV, Siow CC, Tan SY, Old LA, Jakubovics NS, Choo SW. StreptoBase: an oral Streptococcus mitis group genomic resource and analysis platform. PLoS ONE. 2016;11(5): e0151908.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Cobe HM. Transitory bacteremia. Oral Surg Oral Med Oral Pathol. 1954;7(6):609–15.

    Article  CAS  PubMed  Google Scholar 

  63. Silver JG, Martin AW, McBride BC. Experimental transient bacteraemias in human subjects with varying degrees of plaque accumulation and gingival inflammation. J Clin Periodontol. 1977;4(2):92–9.

    Article  CAS  PubMed  Google Scholar 

  64. Hartzell JD, Torres D, Kim P, Wortmann G. Incidence of bacteremia after routine tooth brushing. Am J Med Sci. 2005;329(4):178–80.

    Article  PubMed  Google Scholar 

  65. Forner L, Larsen T, Kilian M, Holmstrup P. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol. 2006;33(6):401–7.

    Article  PubMed  Google Scholar 

  66. Kamate WI, Vibhute NA, Baad RK. Estimation of DMFT, salivary Streptococcus mutans count, flow rate, Ph, and salivary total calcium content in pregnant and non-pregnant women: a prospective study. J Clin Diagn Res. 2017;11(4):ZC147–51.

    PubMed  PubMed Central  Google Scholar 

  67. Romero R, Miranda J, Chaiworapongsa T, Chaemsaithong P, Gotsch F, Dong Z, Ahmed AI, Yoon BH, Hassan SS, Kim CJ, et al. Sterile intra-amniotic inflammation in asymptomatic patients with a sonographic short cervix: prevalence and clinical significance. J Matern Fetal Neonatal Med. 2015;28(11):1343–59.

    Article  PubMed  Google Scholar 

  68. Mores CR, Price TK, Wolff B, Halverson T, Limeira R, Brubaker L, Mueller ER, Putonti C, Wolfe AJ. Genomic relatedness and clinical significance of Streptococcus mitis strains isolated from the urogenital tract of sexual partners. Microb Genom. 2021;7(3):mgen000535.

    PubMed Central  Google Scholar 

  69. Kumar J, Samelson R. Oral health care during pregnancy recommendations for oral health professionals. N Y State Dent J. 2009;75(6):29–33.

    PubMed  Google Scholar 

  70. Boggess KA, Urlaub DM, Massey KE, Moos MK, Matheson MB, Lorenz C. Oral hygiene practices and dental service utilization among pregnant women. J Am Dent Assoc. 2010;141(5):553–61.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Achtari MD, Georgakopoulou EA, Afentoulide N. Dental care throughout pregnancy: what a dentist must know. Oral Health Dent Manag. 2012;11(4):169–76.

    PubMed  Google Scholar 

  72. American College of Obstetricians and Gynecologists. Committee Opinion No. 569: oral health care during pregnancy and through the lifespan. Obstet Gynecol. 2013;122(2 Pt 1):417–22.

    Google Scholar 

Download references

Acknowledgements

We thank the patient for her permission to use the data. We gratefully thank Assistant Professor Anchalee Limrungsikul for in-depth discussion in the management of early-onset neonatal sepsis and current clinical practice guidelines. We sincerely thank staffs at labor and delivery unit, Ramathibodi hospital for cooperation and providing appropriate care to the patient. We finally thank Jitpisuth Tantasiri for proofreading and editing the manuscript.

Funding

This research project is supported by Mahidol University (Basic Research Fund: fiscal year 2022; Grant Number: BRF1-018/2565) and Faculty of Medicine Ramathibodi Hospital Mahidol University. The funding supported the cost of bacterial identification. The funding was not used in any other aspect of the study, including its design, data collection, writing of the report, or decision to submit for publication.

Author information

Authors and Affiliations

Authors

Contributions

PC and PP wrote the first draft of the manuscript. PC, PP, AJ and SP revised the manuscript; PC, WL, and TK collected the clinical samples and clinical information; PS, PM, and PP conducted microbiological identification; AS performed pathological examination. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Piya Chaemsaithong, Arunee Singsaneh or Pisut Pongchaikul.

Ethics declarations

Ethics approval and consent to participate

The patient was enrolled in the systemic characterization of microbiology in preterm labor protocol approved by the ethics committee of the Faculty of Medicine Ramathibodi Hospital Mahidol University (COA.MURA2021/254).

Consent for publication

The woman whose story is told in this case report has provided a written consent for the publication.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chaemsaithong, P., Lertrut, W., Kamlungkuea, T. et al. Maternal septicemia caused by Streptococcus mitis: a possible link between intra-amniotic infection and periodontitis. Case report and literature review. BMC Infect Dis 22, 562 (2022). https://doi.org/10.1186/s12879-022-07530-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12879-022-07530-z

Keywords