MATERNAL-FETAL MEDICINE

Temporal trends and determinants of peripartum hysterectomyin Lombardy, Northern Italy, 1996–2010

Fabio Parazzini • Elena Ricci • Sonia Cipriani •

Francesca Chiaffarino • Renata Bortolus •

Vito Chiantera • Giuseppe Bulfoni

Received: 31 May 2012 / Accepted: 23 August 2012 / Published online: 19 September 2012

� Springer-Verlag 2012

Abstract

Purpose To analyze the temporal trends of peripartum

hysterectomy (PH) in the period 1996–2010 in Lombardy,

Italy.

Methods Using data from the Regional Database, PH

ratios/1,000 deliveries were calculated from 1996 to 2010,

in strata of age and mode of delivery among women resi-

dent in Lombardy, Italy. PH cases were identified search-

ing the database for the ICD-9 and ICD-10 codes for

subtotal and total hysterectomy. PH ratios/1,000 deliveries

in strata of age, mode of delivery and calendar year were

computed. Poisson’s regression analysis was used to test

trend over time.

Results A total of 905 PH and 1,289,163 deliveries were

recorded between 1996 and 2010. The overall PH ratio was

0.70/1,000 deliveries. The PH ratio/1,000 deliveries

increased over time, being 0.57 in 1996 and 0.88/1,000

deliveries in 2010 (P \ 0.0001). After including calendar

year, mode of delivery and maternal age in the Poisson’s

regression equation, no significant linear trend emerged in

the PH ratio over time (P = 0.28). Women who underwent

cesarean section (CS) (CS vs. vaginal delivery: OR 5.66,

95 % CI 4.91–6.54) and older women were at increased

risk of PH (maternal age C40 vs. \30 years: OR 5.66,

95 % CI 4.48–7.15). The frequency of intractable peri-

partum hemorrhage and placenta praevia/accreta, the main

indications for PH, significantly increased over the study

period.

Conclusions In Lombardy, the PH ratio increased

between 1996 and 2010. In our population, rising fre-

quency of CS and older maternal age may explain this

trend.

Keywords Hysterectomy � Peripartum � Temporal trend �Risk factor � Maternal age � Cesarean section

Introduction

Peripartum hysterectomy (PH) is a severe complication of

pregnancy. The indications of PH are generally uterine

rupture and life-threatening obstetric hemorrhage, often

due to uterine atony or placenta praevia or accreta. Its

frequency has been suggested to be used as an indicator of

maternal care [1–3] in industrialized countries, where

maternal deaths are rare.

Several studies reported that PH ratios increased during

the last decades, as for example in the USA [4] from 0.72/

1,000 in 1994–1995 to 0.83/1,000 deliveries in 2006–2007,

in Israeli [5] from 0.40/1,000 in 1988–1994 to 0.95/1,000

F. Parazzini � E. Ricci (&) � S. Cipriani � F. Chiaffarino �G. Bulfoni

Dipartimento Materno-Infantile, Fondazione IRCCS Ca’

Granda, Ospedale Maggiore Policlinico, Universita degli Studi

di Milano, via Commenda 12, 20122 Milan, Italy

e-mail: ed.ricci@libero.it; ricci@epi2004.it

E. Ricci � S. Cipriani � F. Chiaffarino

Epi2004, Gruppo per la Ricerca Epidemiologica,

20100 Milan, Italy

R. Bortolus

SSF Promozione della Ricerca, Azienda Ospedaliera

Universitaria Integrata Verona, Verona, Italy

V. Chiantera

Department of Gynecology and Gynecological Oncology,

Campus Charite Mitte (CCM) and Campus Benjamin Franklin

(CBF), Charite Universitatsmedizin, Berlin, Germany

123

Arch Gynecol Obstet (2013) 287:223–228

DOI 10.1007/s00404-012-2547-4

in 2001–2007, and in the UK [6] a threefold increase

between 1994–2003, as compared to 1983–1993. The main

reported risk factors for PH are maternal age and delivery

by cesarean section (CS) [7–9]. Moreover, previous CS

may lead to an abnormal placentation during subsequent

pregnancies; placenta praevia and accreta are risk factors

for CS and PH [8, 10, 11].

In Italy, the CS rate arose consistently over the last

decades, from 17.5 % in 1992 to 39.8 % in 2007 [12]. In

Lombardy, the most populated Italian region, the frequency

of CS increased from 21.3 to 28.2 % [13]. Likewise,

maternal age at delivery has been steadily increasing in the

last decades [14].

We evaluated the temporal trends of PH ratios during

the period 1996–2010 in Lombardy, an Italian region of

about 10 million inhabitants [15], using data from the

Regional Healthcare Database. We aimed to assess whether

the PH frequency increased and, in this case, whether the

increase was explained by the main determinants’ modifi-

cation over time.

Methods

Since 1991, a standard form has been used to register all

discharges from public or private hospitals in Lombardy.

Data are reported in an Integrated Patients’ Database. This

Data Warehouse contains information on inpatient activity

provided to each patient by any hospital or clinic (public or

accredited private) belonging to the Regional Health Sys-

tem (RHS). The RHS provided reimbursement for hospital

admissions to each regional healthcare structure. The col-

lected data were validated because on the basis of this

information the healthcare providers (both public and pri-

vate) were reimbursed by the RHS for the services deliv-

ered to each patient.

We obtained data regarding all PH and deliveries from

obstetric departments over the period 1996–2010 by the

Lombardy Health Directorate. PH cases were identified

searching the database for the ICD-9 and ICD-10 codes:

68.31, 68.39—subtotal hysterectomy; 68.41, 68.49, 68.51,

68.59, 68.61, 68.69, 68.71, 68.79, 68.8, 68.9—total

hysterectomy.

Information on maternal age and mode of delivery was

obtained for all deliveries. For PH cases, type of hyster-

ectomy (total or subtotal) and indication for surgery were

recorded. PH ratios/1,000 deliveries in strata of age (\30,

30–39, C40 years), mode of delivery (vaginal delivery or

CS) and calendar year were computed. To account simul-

taneously for the effects of mode of delivery, calendar

period and maternal age, we used unconditional multiple

logistic regression, with maximum likelihood fitting, to

obtain odds ratios (OR) and their corresponding 95 %

confidence interval (CI). Poisson’s regression analysis was

used to test trend over time. Statistical significance was set

at P \ 0.05.

All analyses were carried out using SAS/STAT, version

9.1 software (SAS Institute Inc, Cary, NC, USA).

Results

A total of 905 PH and 1,289,163 deliveries were recorded

between 1996 and 2010. The overall PH ratio was 0.70/

1,000 deliveries. During this period, the mean age at

delivery increased, from 30.1 years in 1996 to 31.8 years

in 2010, as well as the CS proportion, from 21.4 to 28.2 %.

The number of PH and ratios/1,000 deliveries are shown in

Table 1.

The PH ratio increased over time, being 0.60 in 1996

and 0.93/1,000 deliveries in 2010 (P \ 0.0001) (Fig 1a).

PH ratios/1,000 deliveries for mode of delivery and age

class are also shown in Fig. 1b and c respectively, over the

1996–2010 period. Women who delivered by CS (OR 5.66,

95 % CI 4.91–6.54) and older women were at increased

risk of PH (maternal age C40 vs. \30 years: OR 5.66,

95 % CI 4.48–7.15). Women who had a twin pregnancy

were at increased risk of PH in the univariate analysis, but

this finding was not statistically significant after adjusting

for maternal age and mode of delivery.

After including in the Poisson’s regression equation

calendar year, mode of delivery and maternal age, no sig-

nificant linear trend emerged in the PH ratio over time

(P = 0.28). The proportion of subtotal PH did not show

marked differences over the period (Table 2). The main

indication for PH was intractable peripartum hemorrhage

(65.7 %), mainly immediately postpartum (48.8 %). PH

due to hemorrhage showed a significant increase over time,

from 48.1 % in the 1996–1998 period to 72.5 % in the

2008–2010 period (P \ 0.0001). Patients with hemorrhage

as the only indication for PH were 352 (38.9 %), a pro-

portion increasing between 1996–1998 (35.1 %) and

2008–2010 (45.3 %).

The indication for surgery ‘‘placenta praevia/accreta’’

also showed a significant increase over the period

(P = 0.03). These findings remained statistically signifi-

cant after adjusting for age class at delivery.

Discussion

This study shows that the frequency of PH in Lombardy

increased over the 1996–2010 period. After taking into

account the effect of mode of delivery and maternal age in

the analysis of time trend, the PH increase over time was

no longer statistically significant.

224 Arch Gynecol Obstet (2013) 287:223–228

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Fig. 1 a Ratio of PH/1,000 deliveries in the 1996–2010 period; b ratio of PH/1,000 vaginal deliveries or cesarean section; c ratio of PH/1,000

deliveries in women aged \30, 30–39 and C40

Table 1 Peripartum

hysterectomy (PH) in

Lombardy, 1996–2010

a 95 % Confidence intervalb For age class, mode of

delivery, singleton/twin

pregnancy, calendar periodc Reference category

No. of PH No. of

deliveries

Ratio/1,000

deliveries

Crude odds

ratioaAdjusted

odds ratioa,b

Calendar period

1996–1998 131 231,480 0.57 1c 1c

1999–2001 134 246,600 0.54 0.96 (0.76–1.22) 0.87 (0.69–1.11)

2002–2004 200 259,156 0.77 1.36 (1.09–1.70) 1.14 (0.91–1.42)

2005–2007 193 271,800 0.71 1.26 (1.01–1.57) 0.98 (0.79–1.23)

2008–2010 247 280,127 0.88 1.56 (1.26–1.93) 1.18 (0.95–1.46)

Maternal age at delivery (years)

\30 147 459,587 0.32 1c 1c

30–39 617 776,622 0.79 2.49 (2.08–2.98) 2.16 (1.80–2.58)

C40 141 52,954 2.66 8.34 (6.62–10.51) 5.66 (4.48–7.15)

Mode of delivery

Vaginal delivery 276 949,274 0.29 1c 1c

Cesarean section 629 339,889 1.85 6.38 (5.53–7.35) 5.66 (4.91–6.54)

Pregnancy

Singleton 876 1,274,002 0.69 1c 1c

Multiple 29 15,161 1.91 2.79 (1.92–4.03) 1.20 (0.83–1.74)

Arch Gynecol Obstet (2013) 287:223–228 225

123

Our data should be considered totally representative of

the cases of PH in the region: in Lombardy all hospital

admissions and surgical procedures are registered by law in

a regional administrative database. With regard to the

quality of diagnosis, for administrative reasons, all medical

records are reviewed, and diagnosis confirmed, by local

medical officers. Among the strengths, we also have to

consider the population-based design and the opportunity

to analyze temporal trends using similar methods of data

collection.

The frequency of PH has been reported to range from

0.24 to 8.9 per 1,000 deliveries, higher ratios being

reported in low income countries [16]. In developed

countries, the PH incidence showed a wide variation,

ranging from 0.2 to 2.28/1,000 deliveries [4, 8, 10, 17–29].

The estimate reported in our population is consistent with

these findings.

Some epidemiological studies have suggested that the

PH frequency is rising. For example, a 25 % increase has

been reported between 1994 and 2006 in the USA [30], as

well as in a population-based study [31] conducted using

the Washington State Birth Certificate Registry in the

period 1987–2006 (from 0.25 to 0.82/1,000 deliveries).

Consistently, in our sample the PH ratio arose by 37 %

(from 0.57 to 0.88/1,000 deliveries) in the 15-year period

between 1996 and 2010.

CS and abnormal placentation [7, 8, 10, 11] are recog-

nized risk factors for PH. The increasing proportion of

abnormal placentation as indication for PH (from 12.9 to

21.5 %), suggested that the rising CS frequency is a risk

factor for PH in subsequent pregnancies, in our population.

The risk of PH was 3.5 time higher in women who had a

previous CS, in a case–control study conducted in the UK

[8], and the risk associated with previous CS was higher

with increasing number of cesarean deliveries (OR 18.6

with 2 or more). In our study, the PH frequency was about

sixfold higher in women delivering by CS in comparison

with vaginal delivery; regrettably, we lack the information

about reproductive history.

In our study, older age was a determinant of higher risk

of PH, consistently with literature [8, 9]. The increase, in

Lombardy, of mean age at delivery (?1.7 years between

1996 and 2010) and CS frequency (from 21.4 to 28.2 %

over the same period) may, at least in part, explain the

Table 2 Type and indication for peripartum hysterectomy (PH)

1996–1998, No.131

(14.3 %)

1999–2001, No.134

(14.8 %)

2002–2004, No.200

(22.2 %)

2005–2007, No.193

(21.4 %)

2008–2010, No.247

(27.2 %)

Total,

No.896

Total PH 85 (66.9) 89 (66.9) 124 (62.3) 135 (73.3) 166 (68.0) 600 (67.0)

Subtotal PH 42 (33.1) 44 (33.1) 75 (37.7) 57 (29.7) 78 (32.0) 296 (33.0)

Indicationa

Hemorrhage 63 (48.1) 77 (57.5) 126 (63.0) 144 (74.6) 179 (72.5) 589 (65.7)

Prepartum 7 (5.3) 10 (7.5) 12 (6.0) 19 (9.8) 10 (4.1) 58 (6.5)

Early

postpartum

43 (32.6) 55 (41.0) 90 (45.0) 103 (53.4) 146 (59.1) 437 (48.8)

Late

postpartum

10 (7.6) 6 (4.5) 14 (7.0) 15 (7.8) 16 (6.5) 61 (6.8)

Unspecified 3 (2.3) 6 (4.5) 10 (5.0) 7 (3.6) 7 (2.8) 33 (3.7)

Coagulopathy 16 (12.2) 17 (12.7) 15 (7.5) 17 (8.8) 17 (6.7) 82 (9.1)

Pelvic

hematoma

3 (2.3) 4 (3.0) 3 (1.5) 1 (0.5) 5 (2.0) 16 (1.8)

Uterine atony 8 (6.1) 10 (7.5) 14 (7.0) 13 (6.7) 7 (2.8) 52 (5.7)

Uterine rupture 11 (8.3) 7 (5.2) 12 (6.0) 9 (4.7) 15 (6.1) 54 (6.0)

Placenta accreta/

previa

16 (12.9) 23 (17.2) 45 (22.5) 44 (22.8) 53 (21.5) 181 (20.0)

Surgical

complication

6 (4.5) 6 (4.5) 7 (3.5) 6 (3.1) 9 (3.6) 34 (3.8)

Obstetric shock 8 (6.1) 8 (6.0) 6 (3.0) 14 (7.2) 15 (6.1) 51 (5.6)

Genital cancer/

fibroids

7 (5.3) 9 (6.7) 22 (11.0) 11 (5.7) 11 (4.4) 60 (6.7)

Sometimes the sum does not add up to the total because of unreported/not defined indicationa Some cases had more than one indication

226 Arch Gynecol Obstet (2013) 287:223–228

123

increase of PH ratios observed in our population. Along

this line, the age- and mode of delivery-adjusted temporal

trend was not statistically significant.

It has also been suggested that PH is more common in

multiple gestation [28]. Overall, we found that, after

adjusting for age and mode of delivery, the effect of

multiple pregnancy was not statistically significant.

Moreover, the estimated OR diminished from 2.79 to 1.20,

possibly indicating that the apparent relationship was due

to a greater proportion of CS in multiple births and older

age of women with twin gestation.

Potential limitations should also be considered. The main

limitation of this analysis was the lack of information on

indication for CS and reproductive history, that prevented us

to analyze some important factors. Moreover, when the

indication for PH was ‘‘hemorrhage’’, we were not able to

further investigate, if missing, the cause of hemorrhage

(uterine atony, placenta praevia/accreta, uterine rupture).

Conclusions

Our data showed that in Lombardy, over a 15-year period,

the PH ratios/1,000 deliveries increased. This trend was

largely explained by the changing frequency of CS and by

the older maternal age observed in our population, over the

1996–2010 period.

Acknowledgments This study was partially funded by Fondazione

IRCCS Ca’ Granda, Ospedale Maggiore Policlinico, in the framework

of ‘‘Fondi Ricerca Corrente’’. The authors thank Dr. Carlo Zocchetti,

Lombardy Region, Health Directorate, for providing data.

Conflict of interest No competing financial interests exist.

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