Hypertension Research in Pregnancy
Online ISSN : 2187-9931
Print ISSN : 2187-5987
ISSN-L : 2187-5987
Original Article
Cesarean delivery “en caul” in Japan: Results of a national survey of maternal and perinatal centers in Japan
Koichiro Takagi Mitsue Muraoka
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2019 年 7 巻 2 号 p. 56-61

詳細
Abstract

Aim: “En caul” cesarean section can prevent mechanical damage to preterm babies upon cesarean delivery, by intentionally not rupturing the fetal membranes. This survey investigates its prevalence, indications, and advantages and disadvantages in Japan.

Methods: Questionnaires were posted to all registered Level 2 and Level 3 maternal and perinatal centers (where most premature babies are delivered) in Japan (n=327). Percentages of centers are presented as survey results.

Results: Response rate was 53.2%. En caul cesarean section was employed in 43.2% and 81.6% of Level 2 and 3 centers, respectively. Gestational age considered for en caul cesarean section was less than 31 weeks in 75.9% of centers. Low transverse and vertical uterine incisions were made at 64% and 29% of centers, respectively. En caul cesarean section was considered useful by 87% of centers. However, nearly one-third of the respondents noted that this procedure presents some technical difficulties if membranes happen to rupture accidentally before the delivery of the fetus is complete.

Conclusions: En caul cesarean section is a routine cesarean delivery technique used for preterm babies born at Level 3 maternal and perinatal centers in Japan. However, certain technical and educational aspects should be considered to achieve better outcomes.

Introduction

With marked advancements made in maternal, fetal, and neonatal medicine, the prognosis of premature infants born in Japan has improved dramatically and is considered among the best in the world.1,2) Perinatal medical services strongly influence these prognoses and are provided primarily at the municipal district level. Japan is divided into nine regions comprising 47 prefectures, each of which has at least one Level 3 institute, i.e., a tertiary perinatal center with maternal and neonatal intensive care units to handle highest risk pregnancies. Each region has several Level 2 perinatal centers with neonatal intensive care units associated with the Level 3 perinatal center in the same region; these cover relatively high-risk pregnancies. Several factors affect the prognoses of premature infants, including antenatal maternal care, delivery room management, postnatal respiratory care, nutrition, infection, and retinopathy care.

Regardless of the indications for cesarean delivery of premature infants, the overall prognosis of infants is better for those born by cesarean than by vaginal delivery.3) Nonetheless, cesarean delivery is not always safe, with an incidence of fetal injury during cesarean delivery of 1.1%.3) More than half of the injuries involve skin lacerations, while others include cephalohematoma, clavicle fracture, facial nerve palsy, brachial plexus injury, intracranial hemorrhage, and long-bone fracture.3) Therefore, less traumatic cesarean delivery techniques for premature infants have been sought.

In 1990, Pearson introduced “en caul” cesarean section (ECC), in which the fetal membranes are intentionally left intact until the whole sac has been delivered, to avoid neonatal injuries during the procedure.4) Eight years later, Abouzeid and Thornton reported an ECC case series based on a postal survey of 78 consultants in the Yorkshire region in the United Kingdom.5) We reported on the introduction of the ECC technique in Japan in 1993,6) leading to its widespread use throughout Japan since then.

In this study, we investigated the extent to which this technique is applied and the problems encountered in its implementation. To this end, we performed a nationwide postal survey targeting maternal and perinatal centers in Japan.

Materials and methods

In 2010, questionnaires were posted to all registered Level 2 and Level 3 maternal and perinatal centers in Japan (n=327). The survey queried whether or not ECC is employed, and if so, the indications to perform ECC, gestational age, fetal growth, and fetal presentation. The number of ECC cases during the year 2010 was also asked, along with primary indications for ECC. Free space for additional comments was also included in the questionnaire.

Results

The overall response rate was 53.2%; response rates were 51.4% for Level 2 and 58.3% for Level 3 centers (Table 1).

Table 1. Number of registered Level 2 and 3 maternal and perinatal centers in Japan
Number of centers and targeted and response ratesLevel 3Level 2Total
Number of perinatal centers84243327
Response (%)49 (58.3)125 (51.4)174 (53.2)

ECC was employed in 43.2% of Level 2 and 81.6% of Level 3 perinatal centers in Japan (Table 2). With regard to indications for ECC, 58 institutions (62%) responded that they considered gestational age an indication for ECC. When ECC was employed according to gestational age, some institutions employed the procedure only for a very young gestational age, whereas others simply employed ECC for any preterm cesarean delivery (Figure 1). Indication for ECC in terms of gestational weeks was considered in nearly half of the institutions; specifically, ECC was considered for those younger than 28 gestational weeks with an estimated birth weight under 1,000 grams (Figures 1 and 2).

Table 2. Rate of implementation of en caul cesarean sectiont
Level 3Level 2Total
“En caul” employed (%)40 (81.6)54 (43.2)94 (54.0)
Figure 1.

Indication for en caul cesarean section by gestational age and cumulative number of institutions

Among the 94 institutions that responded, 19 did not answer this question, 20 answered that they did not consider gestational age, 9 answered that they consider gestational age but did not define a specific cutoff with regard to gestational week.

Figure 2.

Indication for en caul cesarean section by estimated birth weights and cumulative number of institutions

Among the 94 institutions that responded, 23 did not answer this question, 13 did not consider estimated birth weight, and 12 employed en caul cesarean section for all preterm cesarean deliveries.

With regard to the mode of ECC, 29 institutions employ complete ECC (25.5%), 19 institutions employ incomplete ECC (20.2%), and the remaining 30 institutions employ both types of ECC (31.9%) (Figure 2).

The choice of uterine incision (lower segment incision, or classical or vertical incision) is shown in Figure 3. Moreover, 75 institutions (64%) use a lower segment incision, 34 institutions (29%) use the classical vertical incision, and 8 institutions did not respond to this question (Figure 3).

Figure 3.

Mode of “en caul” cesarean section

*Fetal membranes may be intentionally ruptured after most of the body parts are delivered; i.e., incomplete en caul cesarean section.

Figure 4.

Mode of uterine incision in en caul cesarean section

With regard to the application of rapid tocolysis upon ECC, 46 institutions (48.6%) employ nitrate and 7 institutions (7.4%) employ inhalational agents (not specified), while no institutions employed ritodrine hydrochloride. Twenty institutions (21.3%) do not employ tocolysis (Table 3).

Table 3. Rapid tocolysis used during en caul cesarean section
No. institutions%
Nitrate4648.9
Inhalational agent77.4
Ritodrine HCl00
No tocolysis2021.3
No answer2122.3
Total94100

Other comments left in the survey about ECC were as follows. Seventy institutions (74.5%) noted that ECC is beneficial for neonate protection, 33 institutions wrote that it is beneficial for the surgeons, and 2 institutions (2.1%) responded that they performed ECC upon request from the neonatologists (Table 4). With regard to the disadvantages of ECC, 29 institutions (30.9%) answered that it had some disadvantages. Their comments are shown in Table 5; the disadvantages were that it “takes longer time” (8 institutions), is “technically difficult” (14 institutions), has “adverse effects on the neonates” (6 institutions), and has “no evidence” (1 institution).

Table 4. Additional survey comments on the advantages of en caul cesarean section
For neonates
70 (74.5%)
Minimized stress
22 (23.4%)
Prevents damage
35 (37.2%)
Skin damage
Mechanical damage to the brain
Cerebral hemorrhage
Birth asphyxia
Better Apgar score
Prevents the “hug me tight” phenomenon
13 (13.8%)
For surgeons
33 (35.1%)
Ease of delivery
33 (35.1%)
For malpresentation
Placenta previa
Reassuring
Transverse uterine incision possible
At neonatologist’s request
2 (2.1%)

The “hug me tight” phenomenon is a colloquial term that means to “hold someone you love tightly”. In this case, the uterus might hold the baby tightly enough to prevent delivery, despite strong uterine contractions after the rupture of the membranes.

Table 5. Free descriptive comments on the disadvantages of en caul cesarean section
Takes longer
8 (8.5%)
Requires more careful uterine incision (4)
Expulsion of the bag (4)
Technically difficult
14 (14.9%)
Difficult to teach (3)
Incidental membrane rupture (5)
Not applicable in PROM (2)
More bleeding (when nitrate is used) (3)
Difficult to estimate blood loss (1)
Adverse effects on the neonates
6 (6.4%)
Fear of blood loss (1)
Hypothermia when membranes rupture on infant warmer (2)
Hypoxia due to iatrogenic abruptio placentae (3)
OtherNo evidence (1)

Discussion

ECC was first introduced to Japan in 1993; by 2010, more than 80% of Level 3 and nearly half of Level 2 maternal and perinatal centers were employing this technique. Although its contribution to the incredibly low perinatal mortality and morbidity rates of low-birth weight infants in Japan is difficult to demonstrate, the ECC technique is now widely used in maternal and perinatal centers all over Japan and has become common practice in cesarean deliveries of low-birth-weight infants. While indications for ECC varied among the institutions, most employed ECC for very premature cesarean deliveries.

Lin et al. conducted a prospective study of ECC from 2007 to 2008, investigating 24 cases for which either the estimated birth weight was <1,500 g or gestational age was ≤32 weeks.7) They noted that only 3 of 24 infants had hemoglobin levels <15 g/dl; reasons for the anemia were unrelated to ECC and were likely due to the frequent blood sampling in the neonates. In contrast, the retrospective study of 211 ECC cases conducted by Jin et al. compared these to 836 cases of conventional lower segment cesarean section as the control. This comparison revealed a success rate of 66.8% for ECC (141/211), with a significantly higher 5-minute Apgar score in the subgroup of ECC cases for whom gestational age was <32 weeks.8) With respect to anemia, 4 of 121 cases had severe anemia. Thus, neonatal anemia appears to be a possible adverse effect of ECC. Notably, Lin et al.’s series targeted cases of complete ECC, in which the placenta is completely separated and delivered without rupturing the fetal membranes.7) In contrast, the cases in the study by Jin et al. employed partial ECC, i.e., the placenta was not yet separated at the time of delivery.8) Murakoshi advocated autotransfusion from the placenta before rupturing the membranes on the infant warmer, while holding the placenta at a higher position than the infant.9) Our findings are consistent with these reports with respect to the gestational age and the birth weights for the indication of ECC.

Rapid tocolysis during ECC appears to be useful for relaxing the uterus at the moment of delivery of the fetus, with or without rupturing the membranes, and helps to avoid mechanical stress to the infant. Our survey did not reveal the most suitable tocolytic agent specifically for ECC. It would be desirable to propose selection criteria for uterine incision, i.e., vertical or transverse, and whether or not rapid tocolysis should be employed. Addressing these questions is difficult given the retrospective nature of this study. However, rates of the low transverse incision and of the employment of rapid tocolysis are quite close; we speculate that employment of rapid tocolysis may benefit from the use of a transverse uterine incision at earlier weeks of gestation. With regard to the choice to employ complete or incomplete ECC, the questionnaire did not address the intentionality of the doctors to perform complete or incomplete ECC. Some doctors may perform incomplete ECC to prevent artificial placental abruption with complete ECC. In some cases, the procedure may conclude with an incomplete ECC if the membranes rupture during the course of the complete ECC. In our experience, we have found that once the majority of fetal body parts are delivered, it works best to rupture the membranes in order to proceed with the rapid neonatal resuscitation. We would describe a successful ECC as one in which the membranes are peeled gently away from the uterine wall by the surgeon’s palm before fundal pressure is applied to expel the fetus.

In conclusion, ECC has become a routine technique used in cesarean deliveries of preterm babies born in Japan at Level 3 maternal and perinatal centers, where the majority of premature babies are delivered. Some technical and educational issues remain with this technique, and further investigation is needed to achieve better outcomes with ECC.

Acknowledgements

We thank the following institutions who kindly responded to this survey:

Aomori Prefectural Central Hospital, Aomori City Hospital, Hachinohe City Hospital, Hirosaki University School of Medicine & Hospital, Sendai Red Cross Hospital, Public Katta General Hospital, Akita Red Cross Hospital, Osaki City Hospital, Yamagata Saiseikai Hospital, Shonai Hospital, Takeda General Hospital, Tsuchiura Kyodo General Hospital, Dokkyo Medical University, Haga Red Cross Hospital, Saiseikai Utsunomiya Hospital, Gunma University Hospital, Saitama Medical University Saitama Medical Center, Asahi General Hospital, Funabashi Central Hospital, Tokyo Women’s Medical University Yachiyo Medical Center, Japanese Red Cross Katsushika Maternity Hospital, Kyorin University Hospital, Showa University Hospital, Aiiku Hospital, Tokyo Metropolitan Bokutoh Hospital, Japanese Red Cross Medical Center, Keio University Hospital, The Jikei University Hospital, Juntendo University Hospital, St. Luke’s International Hospital, Kanagawa Children’s Medical Center, Kitasato University Hospital, St. Marianna University Hospital, Yokohama City University Medical Center, Yokohama Rosai Hospital, Showa University Yokohama Northern Hospital, Odawara City Hospital, Saiseikai Yokohamashi Tobu Hospital, Nagano Children’s Hospital, Hokushin General Hospital, Niigata City General Hospital, Niigata Prefectural Shibata Hospital, Niigata Prefectural Central Hospital, Toyama University Hospital, Kanazawa University Hospital, Fukui Prefectural Hospital, Fukui Aiiku Hospital, Sugita Genpaku Memorial Obama Hospital, Ogaki Municipal Hospital, Gifu Prefectural General Hospital, Shizuoka Children’s Hospital, Juntendo University Shizuoka Hospital, Seirei Hamamatsu General Hospital, Hamamatsu University Hospital, Yaizu City Hospital, Anjo Kosei Hospital, Kainan Hospital, Okazaki City Hospital, Tosei General Hospital, Toyota Memorial Hospital, Mie Chuo Medical Center, Mie University Hospital, Mie Prefectural General Medical Center, Japanese Red Cross Ise Hospital, Omihachiman Community Medical Center, University Hospital Kyoto Prefectural University of Medicine, Uji Tokusyukai Medical Center, Japanese Red Cross Kyoto Daini Hospital, Mitsubishi Kyoto Hospital, Kyoto-Katsura Hospital, Takatsuki General Hospital, Chibune General Hospital, Osaka Medical College Hospital, Osaka Women’s and Children’s Hospital, Kansai Medical University Hospital, Osaka University Hospital, Saiseikai Suita Hospital, Rinku General Medical Center, Japanese Red Cross Osama Hospital, Osaka City Sumiyoshi Hospital, Hyogo Prefectural Kobe Children’s Hospital, Kobe City Medical Center General Hospital, Hyogo Prefectural Amagasaki General Medical Center, National Hospital Organization Himeji Medical Center, Wakayama Medical University Hospital, Tottori Prefectural Central Hospital, Kurashiki Central Hospital, Okayama Medical Center, Okayama Red Cross General Hospital, Hiroshima City Hiroshima Citizens Hospital, Onomichi General Hospital, Hiroshima University Hospital, Yamaguchi-ken Saiseikai Shimonoseki General Hospital, Tokuyama General Hospital, Iwakuni Clinical Center, Matsuyama Red Cross Hospital, Kochi Health Sciences Center, Kyushu University Hospital, National Hospital Organization Kyushu Medical Center, Fukuoka Tokusyukai Hospital, National Hospital Organization Nagasaki Medical Center, Sasebo City General Hospital, Nagasaki Harbor Medical Center, Kumamoto City Hospital, Oita Prefectural Hospital, Almeida Memorial Hospital, University of Miyazaki Hospital, Miyazaki Prefectural Nobeoka Hospital, Nanbu Medical Center/Nanbu Child Medical Center

Conflicts of Interest

There are no conflicts of interest to disclose.

References
  • 1.   Inoue  H,  Ochiai  M,  Yasuoka  K, et al. Early mortality and morbidity in infants with birth weight of 500 grams or less in Japan. J Pediatr. 2017; 190: 112–117.
  • 2.   Kono  Y,  Yonemoto  N,  Nakanishi  H,  Kusuda  S,  Fujimura  M. Changes in survival and neurodevelopmental outcomes of infants born at <25 weeks` gestation: a retrospective observational study in tertiary centers in Japan. BMJ Paediatrics Open. 2018; 2: e000211.
  • 3.   Alexander  JM,  Leveno  KJ,  Hauth  J, et al. Fetal injury associated with cesarean delivery. Obstet Gynecol. 2006; 108: 885–890.
  • 4.   Pearson  JF. En Caule cesarean section for delivery of the very low birth weight baby. In: Al Azzari F (ed) A Color Atlas of Childbirth & Obstetric Techniques. London, UK: Wolfe Publishing Ltd., 1990; 137–141.
  • 5.   Abouzeid  H,  Thornton  JG. Pre-term delivery by Caesarean section “en caul”. Eur J Obstet Gynecol Reprod Biol. 1998; 84: 51–53.
  • 6.   Takagi  K. En Caule cesarean section. Rinfusan, 1993; 47: 1318–1320.
  • 7.   Lin  CH,  Lin  SY,  Yang  YH, et al. Extremely preterm cesarean delivery “En Caul”. Taiwan J Obstet Gynecol. 2010; 49: 254–259.
  • 8.   Jin  Z,  Wang  X,  Xu  Q,  Wang  P,  Ai  W. Cesarean section en caul and asphyxia in preterm infants. Acta Obstet Gynecol Scand. 2013; 92: 338–341.
  • 9.   Murakoshi  T. Special cesarean section for preterm infants. Perinatal Med. 2015; 45: 1091–1095.
 
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