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Amniotic Infection Syndrome: Nosology and Reproducibility of Placental Reaction Patterns

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Amniotic Infection Syndrome: Nosology and Reproducibility of Placental Reaction Patterns Pediatric and Developmental Pathology 6, 435–448, 2003 DOI: 10.1007/s10024-003-7070-y © 2003 Society for Pediatric Pathology Amniotic Infection Syndrome: Nosology and Reproducibility of Placental Reaction Patterns 1 2 3 RAYMOND W. REDLINE, * ONA FAYE-PETERSEN, DEBRA HELLER, 4 5 6 FAISAL QURESHI, VAN SAVELL, CAROLE VOGLER, AND THE SOCIETY FOR PEDIATRIC PATHOLOGY,PERINATAL SECTION,AMNIOTIC FLUID INFECTION NOSOLOGY COMMITTEE 1Department of Pathology, University Hospitals of Cleveland and Case Western Reserve University, 11100 Euclid Avenue, Cleveland, OH 44106, USA 2Department of Pathology, University of Alabama at Birmingham, Birmingham, AL, USA 3Department of Pathology, University of Medicine and Dentistry of New Jersey—New Jersey Medical School, Newark, NJ, USA 4Pathology Department, DMC University Laboratories, Hutzel Site and Wayne State University, Detroit, MI, USA 5Department of Pathology, Driscoll Children’s Hospital, Corpus Christie, TX, USA 6Department of Pathology, St. Louis University School of Medicine, St. Louis, MO, USA Received July 1, 2002; accepted May 12, 2003; published online September 11, 2003. ABSTRACT 0.2–0.6, fair/moderate; Ͼ 0.6, substantial. Kappa values for the 12 lesions evaluated in 20 cases by the six pathol- Clinically responsive placental examination seeks to pro- ogists were: acute chorioamnionitis/maternal inflamma- vide useful information regarding the etiology, progno- tory response (any, 0.93; severe 0.76; advanced stage, sis, and recurrence risk of pregnancy disorders. The 0.49); chronic (subacute) chorioamnionitis (0.25); acute purpose of this study was to assemble and validate a chorioamnionitis/fetal inflammatory response (any, complete set of the placental reaction patterns seen with 0.90; severe, 0.55; advanced stage, 0.52); chorionic vessel amniotic fluid infection in the hope that this might pro- thrombi (0.37); peripheral funisitis (0.84); acute villitis vide a standardized diagnostic framework useful for (0.90); acute intervillositis/intervillous abscesses (0.65), practicing pathologists. Study cases (14 with amniotic and decidual plasma cells (0.30). Adoption of this clearly fluid infection, 6 controls) were reviewed blindly by six defined, clinically relevant, and pathologically reproduc- pathologists after agreement on a standard set of diag- ible terminology could enhance clinicopathologic corre- nostic criteria. After analysis of initial results, criteria lation and provide a framework for future clinical re- were refined and a second, overlapping set of cases were search. reviewed. Majority vote served as the gold standard. Grading and staging of maternal and fetal inflammatory Key words: amniotic infection syndrome, chorioamnio- responses was found to be more reproducible using a nitis, nomenclature, placenta, reproducibility two- versus three-tiered grading system than a three- versus five-tiered staging system (overall agreement INTRODUCTION 81% vs. 71%). Sensitivity, specificity, and efficiency for The general sequence of pathologic changes ac- individual observations ranged from 67–100% (24/30 Ͼ 90%). Reproducibility was measured by unweighted companying amniotic fluid infection has been rec- kappa values and interpreted as follows: Ͻ 0.2, poor; ognized for some time [1, 2]. Other clinically rele- vant histologic patterns have been added to this *Corresponding author, e-mail: [email protected] basic framework [3–9]. Despite a fairly extensive literature on this topic, there has been little change as possible to that proposed by the College of in the prevailing diagnostic terminology which has American Pathologists consensus group on placen- basically been “acute chorioamnionitis with or tal diagnosis [17]. Tabulated results from the pre- without funisitis.” Recent data has suggested a re- liminary round (round 1) were circulated and dis- lationship between placental inflammation and cussed. Representative photomicrographs of each important clinical outcomes such as neurologic lesion were reviewed at a meeting of the Society for impairment and chronic lung disease [10–12]. This Pediatric Pathology—Perinatal Section. After the has coincided with a more active clinical approach initial review a second revised set of diagnostic to the management of chorioamnionitis and pre- criteria were proposed and agreed upon. Twelve of term labor [13]. These changes have led to the need the original cases were retained, eight new cases for more detailed description, more specific diag- were added (five new cases and three new con- nostic criteria, and greater standardization of di- trols), and the numerical order was changed. This agnostic terminology in this area. second overlapping set of 20 cases was then circu- As in other organ systems, questions have lated for reexamination followed by an analysis of been raised regarding the reliability of placental individual performance and reproducibility (round diagnosis, i.e., the ability of expert placental pa- 2). thologists to agree with each other and with their The revised diagnostic criteria as agreed upon general pathology colleagues [14–16]. With re- by the study participants before the final evalua- newed interest in the clinical significance of pla- tion (round 2) were as follows: cental pathology, the time seems appropriate to introduce more precision and uniformity in pla- Maternal inflammatory responses cental diagnosis. With this in mind, the Perinatal Stage/progression of disease Section of the Society for Pediatric Pathology has Stage 1 (acute subchorionitis/early acute chorion- undertaken an initiative to review, define, and val- itis) ϭ patchy-diffuse accumulations of neutro- idate diagnostic criteria for a number of different phils in the subchorionic plate fibrin (Fig. 1a) placental reaction patterns. The current report pre- and/or membranous chorionic trophoblast layer (a sents the results of the Amniotic Fluid Infection few scattered neutrophils in the lower half of cho- Nosology Committee. rionic plate and/or the membranous chorionic connective tissue are allowed) (Fig. 1b). Stage 2 METHODS (acute chorioamnionitis) ϭ more than a few scat- A study set of 20 cases was assembled from the files tered neutrophils in the chorionic plate or mem- of University Hospitals of Cleveland. Three slides branous chorionic connective tissue and/or the from each case (umbilical cord, placental mem- amnion (Fig. 1c). Stage 3 (necrotizing chorioam- brances, and one full-thickness section of placental nionitis) ϭ degenerating neutrophils (karyorrhe- parenchyma) were selected. Gestational age and xis), thickened eosinophilic amniotic basement placental weight were provided for each case. membrane, and at least focal amnionic epithelial Fourteen placentas were originally diagnosed by degeneration/sloughage (Fig. 1d). one of the pathologists (R.W.R.) with one or more findings consistent with amniotic fluid infection. Grade/intensity The remaining six placentas had other pathologic Grade 1 (mild–moderate) ϭ individual or small diagnoses, but lacked signs of amniotic fluid infec- clusters of maternal neutrophils diffusely infiltrat- tion. Placental reaction patterns relevant to amni- ing amnion, chorionic plate, chorion laevae, and/or otic fluid infection were chosen for evaluation. subchorionic fibrin (Fig. 1c). Grade 2 (severe) ϭ These patterns are described below, summarized three or more chorionic microabscesses (microab- in Table 1, and illustrated in Figures 1–3. All cases scess ϭ confluent neutrophils measuring at least were examined in a blinded fashion by the six 10 ϫ 20 cells in extent) between chorion and members of the study group using a previously decidua in the membranes and/or under the cho- agreed upon set of diagnostic criteria (round 1). rionic plate (Fig. 1e) or a continuous band of Terminology was chosen to correspond as closely confluent chorionic polymorphonuclear leuko- 436 R.W. REDLINE ET AL. Table 1. Placenta reaction patterns related to amniotic fluid infection: nomenclature and definitions Diagnostic categories Suggested diagnostic terminology Definitions Maternal inflammatory response Stage 1—Early Acute subchorionitis or chorionitis PMN in subchorionic fibrin and/or membrane trophoblast (Fig. 1a,b) 2—Intermediate Acute chorioamnionitis Diffuse-patchy PMN in fibrous chorion and/or amnion (Fig. 1c) 3—Advanced Necrotizing chorioamnionitis PMN karyorrhexis, amniocyte necrosis, and/or amnion basement membrane thickening/hypereosinophilia (Fig. 1d) Grade 1—Mild–moderate No special terminology required Not severe as defined below 2—Severe Severe acute chorioamnionitis or with subchorionic Confluent PMN (Ն 10 ϫ 20 cells in extent) between chorion and microabscesses decidua; Ն 3 isolated foci or continuous band (Fig. 1e) Other Chronic (or subacute) chorioamnionitis Subamnionic mononuclear cell infiltrate with occasional PMN (meconium and hemosiderin-laden macrophages excluded) (Fig. 1f) Fetal inflammatory response Stage 1—Early With chorionic vasculitis or umbilical phlebitis Intramural PMN-chorionic vessels and/or umbilical vein (Fig. 2a,b) 2—Intermediate With umbilical vasculitis (one or two arteries Ϯ Intramural PMN-umbilical artery or arteries (Ϯ umbilical vein) (Fig. vein) or umbilical panvasculitis (all vessels) 2c) 3—Advanced With (subacute) necrotizing funisitis or with PMN Ϯ associated debris in concentric bands-rings-halos around concentric umbilical perivasculitis one or more umbilical vessels (Fig. 2d) A MNIOTIC Grade 1—Mild–moderate No special terminology required Not severe as defined below I 2—Severe With a severe fetal inflammatory response
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