Next Article in Journal
Quantitative Risk Assessment of Wind-Supported Transmission of Highly Pathogenic Avian Influenza Virus to Dutch Poultry Farms via Fecal Particles from Infected Wild Birds in the Environment
Next Article in Special Issue
Synergistic Inhibition of Candida albicans by Cranberry Proanthocyanidins and Probiotics: Novel Strategies for Vulvovaginal Candidiasis Treatment
Previous Article in Journal
Leukotoxin A Production and Release by JP2 and Non-JP2 Genotype Aggregatibacter actinomycetemcomitans in Relation to Culture Conditions
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 13
Issue 7
10.3390/pathogens13070570
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Are Chlamydia Trachomatis and Neisseria Gonorrhoeae Screenings in Pregnant Women Being Properly Performed? A Single-Center Retrospective Observational Study in Italy

by
Vito Mondì
1,*,
Jacopo Caravetta
1,
Piermichele Paolillo
1,
Nicola Salce
1,
Chryssoula Tzialla
2,
Barbara Vasapollo
3,4,
Herbert Valensise
3,4,
Manuela Bedetta
1 and
Simonetta Picone
1
1
Neonatology and Neonatal Intensive Care Unit, Policlinico Casilino, Via Casilina 1049, 00169 Rome, Italy
2
Neonatal ad Pediatric Unit, Polo Ospedaliero Oltrepò, ASST Pavia, Via Volturno 14, 27058 Voghera, Italy
3
Department of Surgical Sciences, University of Rome “Tor Vergata”, Via Montpellier 1, 00133 Rome, Italy
4
Obstetrics and Gynecolocy Unit, Policlinico Casilino, Via Casilina 1049, 00169 Rome, Italy
*
Author to whom correspondence should be addressed.
Pathogens 2024, 13(7), 570; https://doi.org/10.3390/pathogens13070570
Submission received: 27 May 2024 / Revised: 27 June 2024 / Accepted: 5 July 2024 / Published: 8 July 2024
(This article belongs to the Special Issue Focus on Cervicovaginal Health: Microbiome, Sexually Transmitted Infections, and Beneficial Microbes: 2nd Edition)
Versions Notes

Abstract

:
A new Italian intersociety position statement on the prevention of ophthalmia neonatorum was published in 2023. In this document, attention was paid to the indications for the screening of gonococcal and chlamydial infections during pregnancy according to the international and national guidelines for the prevention of sexually transmitted infections (STIs). We conducted an observational retrospective study to assess whether the current guidelines for the prevention of STIs are being followed correctly. From February to August 2022, 2507 women nearing childbirth were enrolled. Among them, 42.4% received a swab for Chlamydia and only 0.5% for gonococcus. Concerning the geographical area of origin, most of the screened women came from Western Europe. None of the women who received gonococcal swabs and only 105 women out of 1062 screened for Chlamydia were under 25 years of age. Overall, only seven swabs were positive for Chlamydia, while none were positive for gonococcus. Concerning the age, geographical area of origin, and medical history of the women with a positive screening for Chlamydia, all were over 25 years old, six were from Western Europe, one was from South America, and none had other STIs. Although monocentric in nature, this study shows that the guidelines are not being followed correctly.

1. Introduction

In 2023, a new intersociety document on the prevention of ophthalmia neonatorum (ON) was issued in Italy [1]. ON is a conjunctivitis that occurs in the first month of life and affects 1.6 to 12% of all newborns [2,3,4]. In the past, ON was exclusively associated with eye infection due to Neisseria gonorrhoeae (NG) [5]. Currently, several bacteria are implicated in this disease. NG now accounts for <1% of the reported cases of ON in the United States, while cases due to Chlamydia trachomatis (CT) range from 2% to 40%. Other bacteria, such as Staphylococcus spp., Streptococcus spp., Haemophilus spp., and other Gram-negative bacterial species, account for 30% to 50% of cases [6]. ON is generally a mild disease. The most severe forms of conjunctivitis appear to be caused by NG and CT. Gonococcal ophthalmia occurs in 30% to 50% of infants exposed during birth and born to positive untreated women. In these cases, the disease can rapidly progress to corneal ulceration, globe perforation, and permanent visual impairment [7]. Infants born to women with untreated chlamydia infection at delivery have a 50% risk of acquiring CT, a 30% to 50% risk of developing neonatal conjunctivitis, and a 10% to 20% risk of developing pneumonia [8]. Untreated chlamydial conjunctivitis can be associated with corneal and conjunctival scarring, hemorrhagic conjunctivitis, and loss of vision [9,10,11].
CT and NG are the two most common bacterial sexually transmitted infections (STIs), and they are a major public health concern. When an infected woman is left untreated, vertical transmission can occur at the time of delivery.
In the new intersociety document [1], attention was paid to two different objectives: neonatal ocular prophylaxis and maternal screening. In assessing the need for universal neonatal prophylaxis, prevention strategies used in other states were also analyzed. There is considerable global variability in recommendations on whether to use ophthalmia neonatorum prophylaxis, and the proper agent used [12]. Universal neonatal ocular prophylaxis was discontinued in the United Kingdom in the 1950s and in Australia, Denmark, Norway, and Sweden in the 1980s [13]. As of 2015 (reaffirmed in 2021), the Canadian Pediatric Society no longer recommends routine neonatal prophylaxis [14]. Universal prophylaxis with 0.5% erythromycin ointment is currently recommended in the United States [15]. Through a survey conducted in Italy [16], it was found that prophylaxis was being performed with drugs not recommended by the World Health Organization [17,18]. According to the new intersociety position statement, in Italy, prophylaxis is no longer recommended for all infants at birth, except for those born from unintended pregnancies, mothers at risk of STIs, and mothers from areas with a high prevalence of gonococcal and chlamydial infection [1].
In creating this document, the importance of maternal screening during pregnancy was highlighted by considering the risk factors identified by the Italian Institute of Health (ISS, Istituto Superiore della Sanità), listed in the new guidelines on physiological pregnancy (Table 1) [19].
This retrospective study aimed to evaluate whether the criteria discussed during the writing of the statement were already pre-considered, and therefore whether there was a need for greater awareness of the necessity of adequate maternal screening in the prevention of ON.

2. Materials and Methods

This was a retrospective observational study. All the women near childbirth at term (gestational age (GA) of more than 37 weeks) admitted to the “Policlinico Casilino” hospital from February to August 2022 were enrolled.
The following data were collected anonymously for each woman: age, nationality (country of birth), positivity for sexually transmitted diseases (syphilis, hepatitis B and C, HIV), GA, mode of delivery, and time of rupture of membranes (pROM). Regarding the screening swabs for CT and NG, whether they were performed or not performed and, if performed, whether they were positive or negative was recorded. Data in the medical records refer to investigations not necessarily prescribed by gynecologists working in our hospital. In our study, we considered swabs performed in the third trimester, the only ones noted in the medical records. According to the new ISS guidelines [19], women with risk factors must be swabbed in the first and third trimester, independently of the result of the first trimester swabs. No criteria were specified for which screening was necessary, but it was assessed whether they were evaluated according to the risk factors identified by the ISS [19]. In addition, in women with a positive swab, it was checked whether antibiotic therapy was performed. Neonates born to women with a CT positive swab were followed up in the first two weeks of life to monitor the onset of ON. Neonates born to women with an NG positive swab, whether untreated or inadequately treated, were evaluated by swab and treated.
In the statistical analysis, we compared general data (GA, pROM, type of delivery) of the women included in the study to assess whether there were significant differences in the populations that had or had not been swabbed. Afterward, we evaluated the risk factors included in the new intersociety document and the ISS guidelines. Specifically, it was evaluated whether there was a difference in the number of women who had or had not been screened for CT and NG in relation to their nationality, age, and IST. Finally, it was assessed whether there was a difference in the number of women who had a negative or positive swab for CT or NG in relation to age and STI.
Concerning the statistical analysis, continuous variables were presented as the mean and standard deviation and compared with the Student’s t test. When using a non-parametric test, stratified data were compared with Fisher’s exact test or the Mann–Whitney test, as appropriate. A p-value of ≤0.05 was considered significant. The analysis was performed using SPSS version 20.0.0 (Statistical Analysis System, Chicago, IL, USA).

3. Results

From February to August 2022, 2507 women were enrolled in our study.

3.1. General Data

The median maternal age was 33.6 years. The mean GA at birth was 39.2 weeks.
The majority (86%) of admitted women had citizenship of a Western European country. The geographical distribution of countries is specified in Supplementary File S1. Concerning screening tests, 1455 women (57.6%) had not been tested for CT. Only 13 women (0.5%) received an NG swab (Table 2). All women who had been screened for NG had also been screened for CT. The identification of NG and CT on swabs is based on nucleic acid amplification tests (NAATs).
Overall, only 10 women were positive for STIs (corresponding to 0.6% of the total sample). Specifically, three were positive for syphilis, six for HBV, and one for HIV.

3.2. Screening in Different Populations

When assessing the differences in age, the timing of membrane rupture, and GA between the women who were screened for CT and NG, the only significant difference was in the GA in the group that underwent CT screening (p = 0.05) (Table 3). Comparing the delivery type in the different groups, there were no significant differences (Table 4). Analyzing the nationality of the mother (Table 5) and comparing the origin of women who had been screened for CT, there were no significant differences in the geographical distribution. When evaluating the NG swabs, most of the screened women were from Western Europe (11 out of 13 screened women). The difference in the geographical population’s distribution of women based on those who received NG swabs was significant (p < 0.001).

3.3. Screening Related to Age and STIs

Among the STI-positive women, none were screened for NG and only four (one HIV-positive and 3 HBV-positive) for CT: all four women were negative for CT. On the contrary, all women tested for NG were unaffected by STIs and none of the seven CT-positive women had an STI.
Regarding age, the prevalence of women screened was over 25 years of age. In the group of women aged under 25, only 57 out of 162 were screened for CT (p = 0.05), and none for NG. All 13 women screened for NG (all with negative results) were older than 25 years. Concerning CT swabs, only one woman under 25 years and 6 over 25 years (Table 6 and Table 7) tested positive. In Table 7, the NG swab results in relation to STIs were not included because no women with STIs had undergone NG screening. Hepatitis C was also not included because no women were recorded as positive for HCV.

3.4. Ophthalmia Neonatorum

In our unit, in the first 7–10 days of life, all newborns were routinely evaluated in the outpatient services, regardless of the maternal screening results. Neonates born to women with CT-positive swabs were followed up in the first two weeks of life. No cases of ON were reported during this period despite CT-positive swabs.

4. Discussion

Globally, STIs remain a challenging public health concern. Chlamydial and gonococcal infections are among the most common STIs around the world.

4.1. Chlamydial and Gonococcal Infection in Pregnant Women

The anatomy of women increases their susceptibility to chlamydial and gonococcal infections [20]. Female urogenital anatomy is more exposed and vulnerable to STIs compared to male urogenital anatomy, particularly because the vaginal mucosa is thin, delicate, and easily penetrated by infectious agents [21]. The impact of vertical transmission cannot be ignored [22]. Most cases of STIs are asymptomatic, which leads to the persistence of the infection, and in some cases, the development of complications that may be irreversible or even fatal. In addition to ON, infertility, ectopic pregnancy, premature rupture of membranes, low-birth-weight infants, and preterm delivery have been reported in women of childbearing age and during pregnancy [23,24].
Therefore, as most NG and CT infections are asymptomatic, screening tests are useful for prompt diagnosis [25,26]. Chlamydial and gonococcal infections are diagnosed by detecting these bacteria in urogenital, rectal, oropharyngeal, or ocular secretions [27]. According to the European and CDC guidelines, the detection of CT and NG should be performed using NAATs, which are based on the amplification of the specific bacteria nucleic acid target sequences and are mostly used due to their higher sensitivity [28,29,30].
Gonococcal and chlamydial infections are treated exclusively with antibiotics. In adolescents and adults, the CDC guidelines for the treatment of CT recommend doxycycline 100 mg orally, twice daily, for 7 days [31]. Doxycycline is contraindicated during the second and third trimesters of pregnancy because of the risk of tooth discoloration. Human data have revealed that levofloxacin, even if it presents a low risk for the fetus during pregnancy, is potentially toxic. Conversely, data from animal studies have raised concerns regarding cartilage damage to neonates [32,33,34]. Clinical experience and published studies indicate that azithromycin is safe and effective during pregnancy [35]. The regimens are based on azithromycin 1 g orally; amoxicillin is listed as an alternative therapy for CT for pregnant women at 500 mg orally three times daily for 7 days [31,36,37].

4.2. Epidemiology

The European Centre for Disease Prevention and Control (ECDC) reported 216,508 confirmed cases of CT in 27 EU/EEA countries, with a crude notification rate of 88 cases per 100,000 population. The notification rate is particularly high in women aged between 20 and 24 [38]. Between 1991 and 2021, 11,383 new cases of CT were reported in Italy. Of these, 3484 cases were reported in women. Considering the entire population, the largest number of cases was reported in the age group between 15 and 24 years. Regarding nationality, 20.3% of the total number of CT patients were foreigners (other European countries and Africa) [39]. In 2022, 70,881 cases of NG were notified in 28 European countries, with a crude notification rate of 17.9 per 100,000 population. Among women, the notification rate was 7.2 per 100,000 population (with 13,599 total cases). The largest proportion of cases reported was in the age group 25–34 years [40]. Between 1991 and 2021, 10,597 new NG cases were registered in Italy. Only 5.9% of cases (626 cases) were in women. In the total population of infected subjects, the highest number of cases was reported in subjects aged between 15 and 44 years. As for CT, infected foreigners (23.9% of the total number of cases) came from other European countries and Africa [39]. In a 2022 systematic review analyzing the global prevalence of NG infection in pregnant women, a higher incidence was confirmed in African countries (prevalence index 3.53). In Europe, a prevalence index of 0.52 was shown, with a prevalence of 0.1 in Italy [41]. In a recent study conducted in Brazil, a higher prevalence of CT than NG was found in pregnant women (9.9% vs. 0.6%) [42]. This difference was also found in sub-Saharan (CT 10.8% vs. NG 3.3%) [43] and in European countries (in the Netherlands, CT 1.8% vs. NG 0.4%) [44]. These data confirm what has already been shown in a study evaluating the global prevalence of STIs (CT 3.8% vs. NG 0.9%) [45].

4.3. Adherence to the New Intersociety Document

While our general data showed that an adequate number of women were screened for CT, a very low number were screened for NG. CT screening carried out using a molecular technique via swabbing (endocervical, vaginal, or urethral) [25] and NG screening by vaginal or endocervical swab must be offered to pregnant women with recognized risk factors at the first antenatal visit and during the third trimester [19]. The Italian intersociety position statement [1] is in line with both the ISS [19] and CDC guidelines [33]. In the CDC recommendations [46], the risk factors for STIs are: age < 25 years or age ≥ 25 years are at increased risk for infection (e.g., women aged ≥ 25 years who have a new sex partner, more than one sex partner, a sex partner with concurrent partners, or sex partner who has an STI) [47]. The risk factors determined by the new ISS guidelines [19] are illustrated in Table 1. In the intersociety position statement, originating from areas with a high incidence of STIs was also added as a risk factor [1]. As described above, in the medical records analyzed, there were only reported swabs performed in the third trimester. This confirms failure to adhere to the recommendations. The need for changes (from increased communication with physicians, to changes in the laboratory processes, etc.), was emphasized in a study carried out in the province of Alberta in Canada, where universal screening is recommended in the first trimester, and rescreening in the third trimester in those who resulted positive in the first one, and in those with risk factors. In fact, the authors demonstrated that although universal, screening in the first trimester was not performed on all women [48].
As can be seen from our data, screening in relation to risk factors was not properly followed. Considering that the average age in our hospital was in line with the average age of mothers presenting for childbirth in Italy (33.1 years among Italian women and 31.1 years among foreign citizens) [49], the number of women to be screened in relation to age only is low. Among women ≤ 25 years old (162), only 57 were screened for CT and none for NG. Concerning STIs, only 0.6% of the total number of women included in the study tested positive (diseases tested for included HIV, HBV, syphilis, and HCV). According to the results, in our center, the incidence of women with STIs was low, and those affected by STIs were not routinely screened for CT and NG.
Concerning the risk factor relating to women’s sexual history (Table 1), in Italy there is a cultural background whereby it is difficult for women to declare their sexual history. The questions suggested by the CDC [47] (e.g., “Are you currently having sex of any kind?” and “What kind of sexual contact do you have, or have you had?”) may have limited use in Italy.
In the new statement [1], maternal “origin” also accounts for a risk factor for STIs Our data (Table 5) indicated that CT swabs were performed in about 50% of women from countries with higher risk, whereas NG swabs were practically never performed. Furthermore, it must be considered whether the mother has resided for a long time in a country with a high incidence of CT or NG, shortly before or during pregnancy.
During the study period (February to August 2022), eye prophylaxis in Italy was not yet limited to specific groups of infants, consequentially all infants received antibiotic prophylaxis for the prevention of ON.

5. Conclusions

In this study, we observed that the risk factors for CT and NG screening during pregnancy are not being properly followed. This is highlighted by a remarkably low number of swabs performed for NG (only 13). Although the number of CT swabs is higher, pregnant women were not correctly tested as not all women under the age of 25 were screened, not all women with STIs were screened, and the nationality of the women was not taken into account. Although the number of women enrolled was limited, the sample represented approximately 0.6% of all the deliveries in Italy in 2022 [50]. Therefore, the results of our study may be representative of Italian reality. Properly following the guidelines for performing screening will lead to the prevention of negative outcomes related to CT and NG infection in pregnancy, including but not limited to ON.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/pathogens13070570/s1, File S1: List of the countries subdivided in geographical area.

Author Contributions

Conceptualization, V.M. and C.T.; methodology, V.M.; software, V.M.; validation, C.T. and S.P.; formal analysis, V.M.; investigation, J.C., N.S. and M.B.; resources, J.C. and M.B.; data curation, J.C. and N.S.; writing—original draft preparation, V.M. and C.T.; writing—review and editing, V.M., C.T., B.V., S.P., H.V. and P.P.; supervision, P.P. and H.V. 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 was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Azienda Sanitaria Locale (Local Health Center) Roma 2 (protocol code 0011318/2023 and approved on 19 January 2023).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study. Written informed consent has also been obtained from the patients to publish this paper.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, Vito Mondì, upon reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Tzialla, C.; Auriti, C.; Aversa, S.; Merazzi, D.; Martinelli, S.; Araimo, G.; Massenzi, L.; Cavallaro, G.; Gagliardi, L.; Giuffrè, M.; et al. Intersociety Position Statement on the Prevention of Ophthalmia Neonatorum in Italy. Microorganisms 2023, 12, 15. [Google Scholar] [CrossRef] [PubMed]
  2. Normann, E.K.; Bakken, O.; Peltola, J.; Andréasson, B.; Buhl, S.; Sigg, P.; Nielsen, K. Treatment of Acute Neonatal Bacterial Conjunctivitis: A Comparison of Fucidic Acid to Chloramphenicol Eye Drops. Acta Ophthalmol. Scand. 2002, 80, 183–187. [Google Scholar] [CrossRef] [PubMed]
  3. Teoh, D.L.; Reynolds, S. Diagnosis and Management of Pediatric Conjunctivitis. Pediatr. Emerg. Care 2003, 19, 48–55. [Google Scholar] [CrossRef] [PubMed]
  4. Wagner, R.S.; Aquino, M. Pediatric Ocular Inflammation. Immunol. Allergy Clin. N. Am. 2008, 28, 169–188. [Google Scholar] [CrossRef]
  5. Barsam, P.C. Specific Prophylaxis of Gonorrheal Ophthalmia Neonatorum: A Review. N. Engl. J. Med. 1966, 274, 731–734. [Google Scholar] [CrossRef] [PubMed]
  6. Pickering, L.K.; Baker, C.J.; Kimberlin, D.W.; Long, S.S. American Academy of Pediatrics. Prevention of Neonatal Ophthalmia. In Red Book; Report of the Committee on Infectious Disease; American Academy of Pediatrics: Elk Grove Village, IL, USA, 2012; pp. 880–882. [Google Scholar]
  7. Donham, B.P.; Gibler, W.B. Images in Emergency Medicine. Gonococcal Conjunctivitis. Ann. Emerg. Med. 2008, 52, 16. [Google Scholar] [CrossRef]
  8. Hammerschlag, M.R. Chlamydial and Gonococcal Infections in Infants and Children. Clin. Infect. Dis. 2011, 53, S99–S102. [Google Scholar] [CrossRef] [PubMed]
  9. Chang, K.; Cheng, V.Y.W.; Kwong, N.S. Neonatal Haemorrhagic Conjunctivitis: A Specific Sign of Chlamydial Infection. Hong Kong Med. J. 2006, 12, 27–32. [Google Scholar]
  10. Darville, T. Chlamydia Trachomatis Infections in Neonates and Young Children. Semin. Pediatr. Infect. Dis. 2005, 16, 235–244. [Google Scholar] [CrossRef]
  11. Kapoor, V.S.; Evans, J.R.; Vedula, S.S. Interventions for preventing ophthalmia neonatorum. Cochrane Database Syst. Rev. 2020, 9, CD001862. [Google Scholar] [CrossRef]
  12. Whitcher, J.P.; Srinivasan, M.; Upadhyay, M.P. Corneal Blindness: A Global Perspective. Bull. World Health Organ. 2001, 79, 214–221. [Google Scholar] [PubMed]
  13. Darling, E.K.; McDonald, H. A Meta-Analysis of the Efficacy of Ocular Prophylactic Agents Used for the Prevention of Gonococcal and Chlamydial Ophthalmia Neonatorum. J. Midwifery Womens Health 2010, 55, 319–327. [Google Scholar] [CrossRef] [PubMed]
  14. Moore, D.L.; MacDonald, N.E. Canadian Paediatric Society, Infectious Diseases and Immunization Committee Preventing Ophthalmia Neonatorum. Paediatr. Child. Health 2015, 20, 93–96. [Google Scholar] [PubMed]
  15. Kimberlin, D.W.; Banarjee, R.; Barnett, E.D.; Lynflield, R.; Sawyer, M.H. Secondary Prevention. In Red Book; Report of the Committee on Infectious Disease; American Academy of Pediatrics: Elk Grove Village, IL, USA, 2024; 1131p. [Google Scholar] [CrossRef]
  16. Mondì, V.; Tzialla, C.; Aversa, S.; Merazzi, D.; Martinelli, S.; Araimo, G.; Massenzi, L.; Cavallaro, G.; Gagliardi, L.; Piersigilli, F.; et al. Antibiotic Prophylaxis for Ophthalmia Neonatorum in Italy: Results from a National Survey and the Italian Intersociety New Position Statements. Ital. J. Pediatr. 2023, 49, 117. [Google Scholar] [CrossRef] [PubMed]
  17. WHO Guidelines for the Treatment of Neisseria Gonorrhoeae; WHO Guidelines Approved by the Guidelines Review Committee; World Health Organization: Geneva, Switherland, 2016; ISBN 978-92-4-154969-1. Available online: https://www.who.int/publications/i/item/9789241549691 (accessed on 11 March 2024).
  18. WHO Guidelines for the Treatment of Chlamydia Trachomatis; WHO Guidelines Approved by the Guidelines Review Committee; World Health Organization: Geneva, Switherland, 2016; ISBN 978-92-4-154971-4. Available online: https://www.who.int/publications/i/item/978-92-4-154971-4 (accessed on 11 March 2024).
  19. Istituto Superiore di Sanità. Antenatal Care for Uncomplicated Pregnancy. PART ONE. Section 1—Information for Pregnant Women. Section 2—Screening for Infections in Pregnancy. 2023, Xiii, 248 p. Linea Guida 1/2023 SNLG (in Italian). Available online: https://www.iss.it/documents/20126/9184367/SNLG+1_2023+Gravidanza-fisiologica+Parte-1.pdf/1b3c23be-4578-48f8-277a-88cf0a98de6c?t=1708700731145 (accessed on 12 March 2024).
  20. Van Gerwen, O.T.; Muzny, C.A.; Marrazzo, J.M. Sexually Transmitted Infections and Female Reproductive Health. Nat. Microbiol. 2022, 7, 1116–1126. [Google Scholar] [CrossRef] [PubMed]
  21. 10 Ways STDs Impact Women Differently from Men. 2024. Available online: https://stacks.cdc.gov/view/cdc/149875 (accessed on 20 June 2024).
  22. Moodley, P.; Sturm, A.W. Sexually Transmitted Infections, Adverse Pregnancy Outcome and Neonatal Infection. Semin. Neonatol. 2000, 5, 255–269. [Google Scholar] [CrossRef] [PubMed]
  23. Vallely, L.M.; Egli-Gany, D.; Wand, H.; Pomat, W.S.; Homer, C.S.E.; Guy, R.; Silver, B.; Rumbold, A.R.; Kaldor, J.M.; Vallely, A.J.; et al. Adverse Pregnancy and Neonatal Outcomes Associated with Neisseria Gonorrhoeae: Systematic Review and Meta-Analysis. Sex. Transm. Infect. 2021, 97, 104–111. [Google Scholar] [CrossRef] [PubMed]
  24. Adachi, K.N.; Nielsen-Saines, K.; Klausner, J.D. Chlamydia Trachomatis Screening and Treatment in Pregnancy to Reduce Adverse Pregnancy and Neonatal Outcomes: A Review. Front. Public. Health 2021, 9, 531073. [Google Scholar] [CrossRef]
  25. Detels, R.; Green, A.M.; Klausner, J.D.; Katzenstein, D.; Gaydos, C.; Handsfield, H.H.; Pequegnat, W.; Mayer, K.; Hartwell, T.D.; Quinn, T.C. The Incidence and Correlates of Symptomatic and Asymptomatic Chlamydia Trachomatis and Neisseria Gonorrhoeae Infections in Selected Populations in Five Countries. Sex. Transm. Dis. 2011, 38, 503–509. [Google Scholar] [CrossRef]
  26. Pillay, J.; Wingert, A.; MacGregor, T.; Gates, M.; Vandermeer, B.; Hartling, L. Screening for Chlamydia and/or Gonorrhea in Primary Health Care: Systematic Reviews on Effectiveness and Patient Preferences. Syst. Rev. 2021, 10, 118. [Google Scholar] [CrossRef]
  27. Centers for Disease Control and Prevention. Recommendations for the Laboratory-Based Detection of Chlamydia Trachomatis and Neisseria Gonorrhoeae--2014. MMWR Recomm. Rep. 2014, 63, 1–19. [Google Scholar]
  28. Chan, P.A.; Robinette, A.; Montgomery, M.; Almonte, A.; Cu-Uvin, S.; Lonks, J.R.; Chapin, K.C.; Kojic, E.M.; Hardy, E.J. Extragenital Infections Caused by Chlamydia Trachomatis and Neisseria Gonorrhoeae: A Review of the Literature. Infect. Dis. Obstet. Gynecol. 2016, 2016, 5758387. [Google Scholar] [CrossRef]
  29. Unemo, M.; Lanjouw, E. The “2015 European Guideline on the Management of Chlamydia Trachomatis Infections” Has Now Been Published. Euro Surveill. 2015, 20, 30080. [Google Scholar] [PubMed]
  30. Unemo, M.; Ross, J.; Serwin, A.B.; Gomberg, M.; Cusini, M.; Jensen, J.S. 2020 European Guideline for the Diagnosis and Treatment of Gonorrhoea in Adults. Int. J. STD AIDS 2021, 32, 108–126. [Google Scholar] [CrossRef]
  31. CDC Guidelines CT Treatment. Available online: https://www.cdc.gov/std/treatment-guidelines/chlamydia.htm (accessed on 17 March 2024).
  32. Jacobson, G.F.; Autry, A.M.; Kirby, R.S.; Liverman, E.M.; Motley, R.U. A Randomized Controlled Trial Comparing Amoxicillin and Azithromycin for the Treatment of Chlamydia Trachomatis in Pregnancy. Am. J. Obstet. Gynecol. 2001, 184, 1352–1354; discussion 1354–1356. [Google Scholar] [CrossRef] [PubMed]
  33. Kacmar, J.; Cheh, E.; Montagno, A.; Peipert, J.F. A Randomized Trial of Azithromycin versus Amoxicillin for the Treatment of Chlamydia Trachomatis in Pregnancy. Infect. Dis. Obstet. Gynecol. 2001, 9, 197–202. [Google Scholar] [CrossRef]
  34. Rahangdale, L.; Guerry, S.; Bauer, H.M.; Packel, L.; Rhew, M.; Baxter, R.; Chow, J.; Bolan, G. An Observational Cohort Study of Chlamydia Trachomatis Treatment in Pregnancy. Sex. Transm. Dis. 2006, 33, 106–110. [Google Scholar] [CrossRef]
  35. Briggs, G.; Freeman, R.; Tower, C. Drugs in Pregnancy and Lactation: A Reference Guide to Fetal and Neonatal Risk, 12th ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2021. [Google Scholar]
  36. Phillips Campbell, R.; Kintner, J.; Whittimore, J.; Schoborg, R.V. Chlamydia Muridarum Enters a Viable but Non-Infectious State in Amoxicillin-Treated BALB/c Mice. Microbes Infect. 2012, 14, 1177–1185. [Google Scholar] [CrossRef]
  37. Wyrick, P.B. Chlamydia Trachomatis Persistence in Vitro: An Overview. J. Infect. Dis. 2010, 201 (Suppl. S2), S88–S95. [Google Scholar] [CrossRef] [PubMed]
  38. European Centre for Disease Prevention and Control. Chlamydia. In ECDC. Annual Epidemiological Report for 2022; ECDC: Stockholm, Sweden, 2024; Available online: https://www.ecdc.europa.eu/sites/default/files/documents/CHLAM_AER_2022_Report.pdf (accessed on 12 March 2024).
  39. Le Infezioni Sessualmente Trasmesse: Aggiornamento Dei Dati Dei Due Sistemi Di Sorveglianza Sentinella Attivi in Italia al 31 Dicembre 2021. Not Ist Super Sanità 2023, 36, 3–39. Available online: https://www.iss.it/documents/20126/6683812/Vol.+36,+n.+5.pdf/c7178c1e-667a-a0f5-134c-e22a1c30939d?t=1689688348936 (accessed on 12 March 2024).
  40. European Centre for Disease Prevention and Control. Gonorrhoea. In ECDC. Annual Epidemiological Report for 2022; ECDC: Stockholm, Sweden, 2024; Available online: https://www.ecdc.europa.eu/sites/default/files/documents/GONO_AER_2022_Report%20FINAL.pdf (accessed on 12 March 2024).
  41. Vaezzadeh, K.; Sepidarkish, M.; Mollalo, A.; Asadi, N.; Rouholamin, S.; Rezaeinejad, M.; Mojtahedi, M.F.; Hosseini, S.M.M.; Taheri, M.; Mahjour, S.; et al. Global prevalence of Neisseria gonorrhoeae infection in pregnant women: A systematic review and meta-analysis. Clin. Microbiol. Infect. 2023, 29, 22–31. [Google Scholar] [CrossRef]
  42. Miranda, A.E.; Gaspar, P.C.; Schörner, M.A.; Barazzetti, F.H.; Dias, G.B.; Bigolin, A.; Pascom, A.R.P.; Barreira, D.; Bazzo, M.L.; Brazilian Surveillance for STIs in Pregnant Women Group. Prevalence of Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and Mycoplasma genitalium and risk factors among pregnant women in Brazil: Results from the national molecular diagnosis implementation project. Int. J. Gynaecol. Obstet. 2024, 166, 71–79. [Google Scholar] [CrossRef] [PubMed]
  43. Nyemba, D.C.; Haddison, E.C.; Wang, C.; Johnson, L.F.; Myer, L.; Davey, D.J. Prevalence of curable STIs and bacterial vaginosis during pregnancy in sub-Saharan Africa: A systematic review and meta-analysis. Sex. Transm. Infect. 2022, 98, 484–491. [Google Scholar] [CrossRef] [PubMed]
  44. Op de Coul, E.L.M.; Peek, D.; van Weert, Y.W.M.; Morré, S.A.; Rours, I.; Hukkelhoven, C.; de Jonge, A.; van Benthem, B.; Pereboom, M. Neisseria gonorrhoea, and trichomonas vaginalis infections among pregnant women and male partners in Dutch midwifery practices: Prevalence, risk factors, and perinatal outcomes. Reprod. Health 2021, 18, 132. [Google Scholar] [CrossRef]
  45. Rowley, J.; Vander Hoorn, S.; Korenromp, E.; Low, N.; Unemo, M.; Abu-Raddad, L.J.; Chico, R.M.; Smolak, A.; Newman, L.; Gottlieb, S.; et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: Global prevalence and incidence estimates, 2016. Bull. World Health Organ. 2019, 97, 548–562. [Google Scholar] [CrossRef] [PubMed]
  46. Workowski, K.A.; Bachmann, L.H.; Chan, P.A.; Johnston, C.M.; Muzny, C.A.; Park, I.; Reno, H.; Zenilman, J.M.; Bolan, G.A. Sexually Transmitted Infections Treatment Guidelines. Sex. Transm. Infect. Treat. Guidel. 2021, 70, 1–184. [Google Scholar]
  47. Cantor, A.; Dana, T.; Griffin, J.C.; Nelson, H.D.; Weeks, C.; Winthrop, K.L.; Chou, R. Screening for Chlamydial and Gonococcal Infections: Updated Evidence Report and Systematic Review for the US Preventive Services Task Force. JAMA 2021, 326, 957–966. [Google Scholar] [CrossRef]
  48. McCullough, E.; Gratrix, J.; Smyzcek, P.; Charlton, C.; Plitt, S.S. Retrospective Review of Prenatal Gonorrhea and Chlamydia Screening in Alberta: 2018–2022. J. Obstet. Gynaecol. Can. 2024, 46, 102229. [Google Scholar] [CrossRef]
  49. Certificato di Assistenza al Parto (CeDAP). Analisi Dell’evento Nascita. Anno 2022. Available online: https://www.salute.gov.it/imgs/C_17_pubblicazioni_3346_allegato.pdf (accessed on 13 March 2024).
  50. Natalità e Fecondità Della Popolazione Residente. Anno 2022 Dati ISTAT. Available online: https://www.istat.it/it/files//2023/10/Report-natalita-26-ottobre-2023.pdf (accessed on 13 March 2024).
Table 1. Risk factors for STIs in pregnant women issued by the Italian Ministry of Health [19].
Table 1. Risk factors for STIs in pregnant women issued by the Italian Ministry of Health [19].
ParameterRisk Factor
Age<25 years
Sexual partnerNew sexual partner (within 3 months)
Multiple sexual partners
Sexual partner with an STI
Sexual protectionNot using barrier protection properly in a non-reciprocal monogamous relationship
STIsHaving an STI
Sexual intercourseOffering sexual intercourse in exchange for money or drugs
Table 2. General data: type of delivery, geographical nationality, gestational age of delivery, time of membrane rupture (pROM), maternal age (years), and number of women who received chlamydial or gonococcal swab. ΔS: deviation standard; ws: weeks; h: hours; ys: years.
Table 2. General data: type of delivery, geographical nationality, gestational age of delivery, time of membrane rupture (pROM), maternal age (years), and number of women who received chlamydial or gonococcal swab. ΔS: deviation standard; ws: weeks; h: hours; ys: years.
Delivery (n°, %)Vaginal delivery: 1243 (49.6%)
Planned Cesarean section: 626 (25%)
Urgent Cesarean section: 392 (15.6%)
Operative vaginal delivery: 246 (9.8%)
Geographical nationality (n°, %)Western Europe: 2155 (86%)
Eastern Europe: 181 (7.2%)
South Asia: 45 (1.8%)
Central and South America: 39 (1.6%)
North Africa: 31 (1.2%)
Remaining Africa: 29 (1.2%)
South-East Asia and the Far East: 13 (0.5%)
North America: 6 (0.2%)
Russia and Central Asia: 6 (0.2%)
Middle East: 2 (0.1%)
Gestational Age (ws ± ΔS)39.2 ± 1.2
pROM (h ± ΔS)3.8 ± 5.6
Maternal age (ys ± ΔS)33.6 ± 5.4
Chlamydial swab (n°, %)Negative: 1055 (42.1%)
Positive: 7 (0.3%)
Not screened: 1445 (57.6%)
Gonococcal swab (n°, %)Negative: 13 (0.5%)
Positive: 0
Not screened: 2494 (99.5%)
Table 3. Comparison of mean gestational age (weeks), time of membrane rupture (pROM) (hours), and maternal age (years) in groups of women who had or had not been screened for chlamydia or gonococcus. ΔS: deviation standard.
Table 3. Comparison of mean gestational age (weeks), time of membrane rupture (pROM) (hours), and maternal age (years) in groups of women who had or had not been screened for chlamydia or gonococcus. ΔS: deviation standard.
Gestational Age
(Weeks, Median ± ΔS)		pProm
(Hours, Median ± ΔS)		pMother Age
(Years, Median ± ΔS)		p
CHLAMYDIAL SWAB
Not screened (1445)39.2 ± 1.20.054 ± 5.80.0733.6 ± 5.50.18
Screened (1062)39.1 ± 1.33.6 ± 5.333.8 ± 5.3
GONOCOCCAL SWAB
Not screened (2494)39.2 ± 1.20.803.8 ± 5.60.533.7 ± 5.40.93
Screened (13)39.1 ± 1.52.6 ± 3.834 ± 4.8
Table 4. Comparison of delivery types and screening.
Table 4. Comparison of delivery types and screening.
DELIVERY
Vaginal DeliveryPlanned Cesarean SectionUrgent Cesarean SectionOperative Vaginal DeliveryTotalp
CHLAMYDIAL SWAB0.294
Screened540 (21.5%)267 (10.7%)149 (5.9%)106 (4.2%)1062 (42.4%)
Not screened703 (28%)359 (14.3%)243 (9.7%)140 (5.6%)1445 (57.6%)
TOTAL1243 (49.5%)626 (25%)392 (15.6%)246 (9.8%)2507 (100%)
GONOCOCCAL SWAB0.988
Screened7 (0.3%)3 (0.1%)2 (0.1%)1 (0.1%)13 (0.6%)
Not screened1236 (49.2%)623 (24.9%)390 (15.5%)245 (9.7%)2494 (99.4%)
TOTAL1243 (49.5%)626 (25%)392 (15.6%)246 (9.8%)2507 (100%)
Table 5. Distribution based on maternal nationality.
Table 5. Distribution based on maternal nationality.
NATIONALITY (DIVIDED INTO GEOGRAPHIC AREAS)
Western EuropeEastern EuropeNorth AfricaCentral and South AfricaNorth AmericaCentral and South AmericaMiddle EastRussia and Central AsiaSouth-East Asia and Far EastSouth AsiaTotalp
CHLAMYDIAL SWAB
Screened897 (35.8%)80 (3.2%)15 (0.6%)15 (0.6%)2 (0.1%)23 (0.9%)2 (0.1%)1 (0.1%)4 (0.2%)23 (0.9%)1062 (42.4%)0.14
Not screened1258 (50.1%)101 (4%)16 (0.6%)14 (0.6%)4 (0.2%)16 (0.6%)05 (0.2%)9 (0.4%)22 (0.9%)1445 (57.6%)
TOTAL2155 (85.9%)181 (7.2%)31 (1.2%)29 (1.2%)6 (0.3%)39 (1.5%)2 (0.1%)6 (0.3%13 (0.6%)45 (1.8%)2507 (100%)
GONOCOCCAL SWAB
Screened11 (0.4%)1 (0.1%)000001 (0.1%)0013 (0.6%)<0.001
Not screened2144 (85.2%)180 (7.1%)31 (1.2%)29 (1.2%)6 (0.2%)39 (1.6%)2 (0.1%)5 (0.2%) 13 (0.6%)45 (1.8%)2494 (99.5%)
TOTAL2155 (85.6%)181 (7.2%)31 (1.2%)29 (1.2%)6 (0.2%)39 (1.6%)2 (0.1%)6 (0.3%)13 (0.6%)45 (1.8%)2507 (100%)
Table 6. Distribution of women screened or not screened according to STI status and age. Yo: years old.
Table 6. Distribution of women screened or not screened according to STI status and age. Yo: years old.
CHLAMYDIAL SWAB
ScreenedNotScreenedp
STI-positive4 (0.2%)6 (0.3%)0.876
STI-negative1058 (42.2%)1439 (57.3%)
>25 yo1005 (40%)1340 (53.4%)0.05
≤25 yo57 (2.3%)105 (4.3%)
GONOCOCCAL SWAB
ScreenedNotScreenedp
STI-positive010 (0.4%)0.81
STI-negative13 (0.6%)2484 (99%)
>25 yo13 (0.6%)162 (6.5%)0.34
≤25 yo02332 (92.9%)
Table 7. Distribution of negative or positive results for CT or NG conducted in women with STIs and distribution of negative or positive results for CT or NG conducted in relation to maternal age. Yo: years old.
Table 7. Distribution of negative or positive results for CT or NG conducted in women with STIs and distribution of negative or positive results for CT or NG conducted in relation to maternal age. Yo: years old.
CHLAMYDIAL SWAB
NegativePositivep
HBV30not evaluable
HIV10
LUE00
CHLAMYDIAL SWAB
NegativePositivep
>25 yo99960.29
≤25 yo561
GONOCOCCAL SWAB
NegativePositivep
>25 yo00not evaluable
≤25 yo130
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Mondì, V.; Caravetta, J.; Paolillo, P.; Salce, N.; Tzialla, C.; Vasapollo, B.; Valensise, H.; Bedetta, M.; Picone, S. Are Chlamydia Trachomatis and Neisseria Gonorrhoeae Screenings in Pregnant Women Being Properly Performed? A Single-Center Retrospective Observational Study in Italy. Pathogens 2024, 13, 570. https://doi.org/10.3390/pathogens13070570

AMA Style

Mondì V, Caravetta J, Paolillo P, Salce N, Tzialla C, Vasapollo B, Valensise H, Bedetta M, Picone S. Are Chlamydia Trachomatis and Neisseria Gonorrhoeae Screenings in Pregnant Women Being Properly Performed? A Single-Center Retrospective Observational Study in Italy. Pathogens. 2024; 13(7):570. https://doi.org/10.3390/pathogens13070570

Chicago/Turabian Style

Mondì, Vito, Jacopo Caravetta, Piermichele Paolillo, Nicola Salce, Chryssoula Tzialla, Barbara Vasapollo, Herbert Valensise, Manuela Bedetta, and Simonetta Picone. 2024. "Are Chlamydia Trachomatis and Neisseria Gonorrhoeae Screenings in Pregnant Women Being Properly Performed? A Single-Center Retrospective Observational Study in Italy" Pathogens 13, no. 7: 570. https://doi.org/10.3390/pathogens13070570

APA Style

Mondì, V., Caravetta, J., Paolillo, P., Salce, N., Tzialla, C., Vasapollo, B., Valensise, H., Bedetta, M., & Picone, S. (2024). Are Chlamydia Trachomatis and Neisseria Gonorrhoeae Screenings in Pregnant Women Being Properly Performed? A Single-Center Retrospective Observational Study in Italy. Pathogens, 13(7), 570. https://doi.org/10.3390/pathogens13070570

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop