Perinatal parameters influenced by recession and migration: an interesting contrast

Ariadne Malamitsi-Puchner Professor of Pediatrics-Neonatology National and Kapodistrian University of Athens Contents

• The crucial perinatal parameters

• The Greek paradigm

• The impact of economic crisis/recession

• The impact of migration flows

• The interesting contrast

Crucial perinatal parameters

- birth weight - - maternal age - mode of delivery The Greek paradigm

Hellenic Statistical Authority

Evolution of births in Greece

1932 185.523 1940 179.500 1955 154.263 1960 157.239 1970 144.928 1980 148.134 1985 116.481 1990 102.229 1995 101.495 2000 103.274 2005 107.545 2006 112.042 2007 111.926 2008 118.302 2009 117.933 2010 114.766 2011 106.428 2012 100.371 2013 94.134 2014 92.149 2015 91.847

Mean birth weight in Greece 2000 – 2015 3.300

3.200

3.100

3.000 2000 2005 2010 2015 Hellenic Statistical Authority

Mean gestational age in Greece 2000 – 2015 39

38,5

38 2000 2005 2010 2015 Hellenic Statistical Authority

Mean maternal age at birth in Greece 1975 – 2015 32 31

30

29

28

27

26

25

24

23 1975 1980 1985 1975 1995 2000 2005 2010 2015

Hellenic Statistical Authority

Total fertility rate in Greece 1975 – 2015

2,6

2,4

2,2

2,0

1,8

1,6

1,4

1,2

1,0

Hellenic Statistical Authority

Age group fertility rate in Greece 1975 - 2015

18

16

14

12

10

8

6

4

2

0 1975 1980 1985 1990 1995 2000 2005 2010 2015

15-19 20-24 25-29 30-34 35-39 40-44

Hellenic Statistical Authority Age specific fertility rates in Greece 1975 and 2015

18

16

14

12

10

8

6

4

2

0 <15 20 25 30 35 40 45 50

1975 2015 Hellenic Statistical Authority Our own studies

Background Background-1 • Economic crises negatively affect population’s status

• Increased risk for somatic, psychological and behavioral morbidity/mortality

• Impact of crisis on health raises concerns for long-term implications

Catalano R et al Annu Rev Public Health 2011;32:431-50 Rajmil L et al Int J Environ Res Public Health 2014;11(6):6528-46 Sdona E et al J Matern Fetal Neonatal Med. 2017

Background-2

• In Greece between 2008 and 2010/12/14→

- GDP declined by 18%

- Total unemployment tripled(7.8% →24.4%)

- Emigration of young people increased

- Fertility rate decreased by 20%

- mortality increased by 41% (2.7-3.8‰)

- Low-birth-weight neonates increased by 19%

OECD 2016 Hellenic Statistical Authority [Accessed 19 Jan. 2017]

Background-3

• Low birth weight (WHO) <2500 g→

At population level→ important indicator of: - long-term maternal malnutrition - ill health - poor health care

At individual level → important predictor of: - neonatal mortality and morbidity - inhibited growth/cognitive development - chronic diseases later in life (DOHaD consequences)

UNICEF, New York, 2004

Background-4 • During last decades Greece: recipient country for a large number of immigrants

• Immigrants from different countries fled to Greece due to:

- collapse of communist regimes (Albania, former Soviet Union)

- civil/other wars, armed conflicts (Pakistan, Afghanistan, Iraq, Syria)

- political dissidence and persecution by dictatorships, martial law regimes (African countries, Philippines)

WHO 2015, OECD2016

Background-5 • Human Development Index-HDI (UN development program) classifies countries based on

- life expectancy - education - per capita income as

- very high - high - medium - low UNDP 2010

Background-6

• Socioeconomic disparities related to adversely affect health

• The “healthy immigrant paradox” refers to immigrants to western countries presenting more favorable health outcomes than the native counterparts

Ray JG et al Can Med Assoc J. 2007 Teruya SA et al Hisp J Behav Sci. 2013 Sdona E et al J Matern Fetal Neonatal Med. 2017 Hypothesis-Aim Hypothesis

Worsening of socioeconomic conditions associated with the crisis, as well as massive migratory flows would negatively affect perinatal health Aim-1

a) To examine primarily changes in: - birth weight - gestational age - maternal age - mode of delivery using individual-level data from 2005 to 2014 b) To explore the possible impact of the economic crisis, manifested in 2008

Aim-2

• To test the “healthy immigrant paradox” and investigate the influence of immigration on major perinatal parameters, as - gestational age - birth weight - mode of delivery taking into account: - maternal age at gestation (primary factor related to fertility)

Subjects-Methods Subjects • Study sample:

- 14,923 neonates during a 10 year period (January 1, 2005 to December 31, 2014) born in a public maternity hospital in Athens, Greece

- mean (SD) gestational age: 38.2 (1.8) w - mean (SD) birth weight: 3157 (532) g - mean (SD) maternal age: 31.6 (4.9) y

Demographic data

Ethnicity Greeks 68.6% Immigrants 31.4%

Male gender N (%) 5257 (51.8%) 2028 (51.5%)

Maternal age (y) mean(SD) 32.4 (4.5) 29.2 (5.3)* [95% CI] [32.3-32.5] [29.1-29.4]

Birth weight (g) mean(SD) 3126 (5289) 3244 (507)* [95% CI] [3116-3136] [3228-3260]

Gestational age (w) 38.2 (1.8) 38.5 (1.7)* mean(SD) [38.1-38.2] [38.5-38.6] [95% CI]

* p <0.05 Methods-1

• Information on:

- date of birth - gender - birth weight - gestational age - maternal age - mode of delivery

• Use of Epidata software (Epidata, Denmark, version 3.1)

Methods-2

• Year 2008: starting point of Greek economic crisis→ first year of GDP decline

• Year 2008: excluded from analysis, due to a cluster of neonates with NEC → led to closure of unit for a month

Methods-3

• Immigrants classified by country of origin in: high, medium, low Human Development Index (HDI) clusters • Greeks served as controls • Comparison of results between Greeks and immigrants • Stratified analysis by maternal age (subgroups of < and > 35 years)

Statistical analysis-1

• Univariable analyses tested: association of study variables - maternal (age, delivery mode) and - neonatal (gender, birth weight, gestational age) with time-periods: 2005-2007, 2009-2011 and 2012-2014

• Multivariable logistic regression analysis identified: factors independently associated with - low birth weight - prematurity - Cesarean Section (CS)

• Statistical significance set at p<0.05

• Use of Stata statistical software (Stata Corporation, Texas, version 11) Characterization of periods

• 2005-2007: before crisis period • 2009-2011: initial crisis period • 2012-2014: established crisis period Statistical analysis-2

• Student’s t-test: to compare sample means • Chi-square test: to compare proportions

• Statistical significance: p<0.05 • Analysis performed by EpiData software Results Results-1 Results-2 Study variables by 3-year-period

Birth weight Gestational age Maternal Caesarean Year Mean (SD) Mean (SD) age section Mean (SD) N (%)

2005-2007 3145.35 (506.46) 38.23 (1.71) 30.94 (4.88) 1885 (43.2) N=4368

2009-2011 3169.99 (537.85) 38.29 (1.88) 31.59 (4.91) 2789 (52.0) N=5376

2012-2014 3142.28 (556.24) 38.13 (1.92) 32.53 (4.94) 2098 (54.8) N=3828 Results-3 Low birth weight and CS rate per year

14 54,9 54,2 55,5 60,0 52,0 49,0 54,8 % low BW 12 44,2 11,5 50,0 % CS 41,8 43,2 42,6 10

10,5 40,0

9,4 9,4 8 9,5 8,6 8,6 7,9 30,0 7,4

6 Birth Weight Birth

6,7 20,0

4 % Low %

10,0 Section Caesarean % 2

0 0,0 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 Year Results-4 Univariable analysis

Low birth weight Prematurity Maternal age (< 2.5 kg) (< 37 w) (≥ 35 y) Year Crude RR Crude RR Crude RR Crude RR N (%) (95%CI) N (%) (95%CI) N (%) (95%CI) N (%) (95%CI)

2005-2007 368 REF 404 REF 1004 REF 1885 REF (N=4368) (8.4) (9.7) (23.3) (43.2) 2009-2011 461 1.024 503 0.971 1505 1.216 2789 1.203 (N=5376) (8.6) (0.898-1.167) (9.4) (0.857-1.099) (28.3) (1.135-1.303)# (52.0) (1.153-1.256)#

2012-2014 398 1.238 429 1.163 1340 1.510 2098 1.270 (N=3828) (10.5) (1.082-1.417)# (11.2) (1.023-1.323)# (35.1) (1.409-1.618)# (54.8) (1.214-1.327)#

# p < 0.05 Results-5 Multivariable analysis Low birth weight Prematurity Caesarean section

(<2.5 Kg) (<37 wk) Adjusted RR Adjusted RR Adjusted RR (95%CI) (95%CI) (95%CI) Predictive factor N=12632 N=12539 N=12625 Year (period) of birth 2005-2007 Ref. Ref. Ref. 2009-2011 0.99 (0.87–1.13) 0.94 (0.83-1.07) 1.17 (1.13–1.22)# 2012-2014 1.16 (1.01–1.33)# 1.09 (0.96-1.24) 1.21 (1.16–1.26)# Maternal age <30 Ref. Ref. Ref. 30-34 1.28 (1.11–1.48)# 1.23 (1.07–1.41)# 1.13 (1.09–1.18)# ≥35 1.82 (1.58–2.09)# 1.82 (1.59–2.08)# 1.23 (1.18–1.29)# Gender NA NA Male Ref Female 1.27 (1.14-1.41)# Low birth weight (< 2.5Kg) NA NA No Ref. Yes 1.60 (1.55–1.65)# Results-6

• Almost one third of mothers were immigrants

• Main countries of immigrant origin (>1%): - Albania HDI: high - Syria HDI: medium - Rumania HDI: high - Pakistan HDI: medium - Former Soviet Union HDI: high - Ethiopia HDI: low - Moldova HDI: medium - Bangladesh HDI: low - Philippines HDI: medium - Burkina Faso HDI: low - Ghana HDI: low

• HDI of immigrants’ countries: HDI of Greeks - high (19.6% of study sample) - very high (68.6%) - medium (6.4% of study sample) - low (0.4% of study sample) -undefined

Results-7

Variables Greeks Immigrants HHDI MHDI LHDI N=10152 N=3940 N=2924 N=953 N=63 Mean (SD) Mean (SD) Mean (SD) Mean (SD) Mean (SD) [95% CI] [95% CI] [95% CI] [95% CI] [95% CI] Maternal 32.4 (4.5) 29.2 (5.3)* 28.9 (5.1)* 30.1 (5.6)* 31.3 (5.2) age [32.3-32.5] [29.1-29.4] [28.7-29.1] [29.8-30.5] [29.9-32.6] (years)

Birth 3126 (5289) 3244 (507)* 3270 (508)* 3173 (498)* 3078 (440) weight [3116-3136] [3228-3260] [3252-3289] [3141-3205] [2967-3189] (grams)

Gestational 38.2 (1.8) 38.5 (1.7)* 38.5 (1.7)* 38.5 (1.6)* 38.3 (1.6) age [38.1-38.2] [38.5-38.6] [38.5-38.6] [38.4-38.6] [37.9-38.7] (weeks)

* p <0.05 Results-8 Variables Greeks Immigrants HHDI MHDI LHDI N=10152 N=3940 N=2924 N=953 N=63 n (%) n (%) n (%) n (%) n (%) [95% CI] [95% CI] [95% CI] [95% CI] [95% CI] Caesarean 5165 (50.9 %) 1750 (44.4 %)* 1314 (44.9 %)* 405 (42.5 %)* 31 (49.2%) section [50.0-51.9] [42.9-46.0] [43.2-46.8] [39.4-45.6] [36.5-61.9] (CS)

Repeat CS 1815 (37.0 %) 709 (43.1 %)* 514 (41.6 %)* 181 (46.9 %)* 14 (58.3 %)

[35.7-38.4] [40.7-45.5] [38.9-44.4] [41.9-51.9] [37.1-79.6]

Multiple 634 (6.4 %) 128 (3.3 %)* 87 (3.1 %)* 41 (4.4 %)* 0 births [5.9-6.9] [2.7-3.9] [2.4-3.7] [3.1-5.7]

* p <0.05 Results-9

Maternal age (years) Greeks Immigrants Total N (%) N (%) N (%)

< 20 25 (0.2) 63 (1.6) 88 (0.6) 20-24 361 (3.6) 720 (18.4) 1081 (7.7) 25-29 2121 (21.1) 1288 (33.0) 3409 (24.4) 30-34 4367 (43.4) 1163 (29.8) 5530 (39.6) 35-39 2598 (25.8) 534 (13.7) 3132 (22.4) 40-44 525 (5.2) 130 (3.3) 655 (4.7) ≥45 58 (0.6) 7 (0.2) 65 (0.5) Total N (%) 10055 (100.0) 3905 (100.0) 13960 (100.0) Results-10

Birth Greeks Immigrants Crude RR Adjusted RR weight (kg) N (%) N (%) p-value (95% CI) (95% CI)

< 2.5 970 (9.7) 241 (6.2) p < 0.001 RR = 0.64 RR = 0.68

≥ 2.5 9032 (90.3) 3648 (93.8) (95% CI: 0.63-0.65) (95% CI: 0.62-0.74)

< 35 years

< 2.5 597 (8.7) 175 (5.4) p < 0.001 RR = 0.62

≥ 2.5 6241 (91.3) 3045 (94.6) (95% CI: 0.58-0.67)

≥ 35 years

< 2.5 373 (11.8) 66 (9.9) p= 0.1558 RR = 0.84

≥ 2.5 2791 (88.2) 603 (90.1) (95% CI: 0.65-1.07) Results-11

Gestational Greeks Immigrants Crude RR Adjusted RR age (weeks) N (%) N (%) p-value (95% CI) (95% CI)

< 37 1036 (10.4) 292 (7.6) p < 0.001 RR = 0.73 RR = 0.77

≥ 37 8899 (89.6) 3570 (92.4) (95% CI: 0.70-0.75) (95% CI: 0.71-0.84)

< 35 years

< 37 618 (9.1) 217 (6.8) p < 0.001 RR = 0.75

≥ 37 6169 (90.9) 2979 (93.2) (95% CI: 0.69-0.80)

≥ 35 years

< 37 418 (13.3) 75 (11.3) p= 0.1587 RR = 0.85

≥ 37 2730 (86.7) 591 (88.7) (95% CI: 0.67-1.07) Results-12

Mode of Greeks Immigrants Crude RR Adjusted RR delivery N (%) N (%) p-value (95% CI) (95% CI)

Vaginal 4926 (49.0) 2170 (55.6) p < 0.001 RR = 0.87 RR = 0.89

CS 5119 (51.0) 1733 (44.4) (95% CI: 0.87-0.88) (95% CI: 0.88-0.91)

< 35 years

Vaginal 3592 (52.3) 1822 (56.4) p < 0.001 RR = 0.91

CS 3275 (47.7) 1410 (43.6) (95% CI: 0.91-0.92)

≥ 35 years

Vaginal 1334 (42.0) 348 (51.9) p < 0.001 RR = 0.83

CS 1844 (58.0) 323 (48.1) (95% CI: 0.76-0.90) Discussion

Discussion -1 • Decreasing birth weight → mainly results from ↑ high-risk pregnancies ↑ premature births evidence exists that ↑ maternal age may influence placental development and permanently change/ “program” fetal growth (Barker 1997)

Discussion-2

• Recent economic crisis left imprint on fertility patterns due to - increased poverty - unemployment - labor market uncertainties disproportionately affecting young people (Goldstein 2013)

Discussion-3

• This study may indicate the presence of supplier-induced demand for CS (financial and convenience incentives) [Gruber and Owings (1996)]

Conclusions-Contrast Conclusions-1 -Contrast

• In Greece 2008-2014 → • Migrants, from countries with significant increase of: high and medium HDI

- Low-birth-weight (<2.5 kg) - ↑ mean birth weight from 6.7% to 11.5% - 48% ↓ risk for <2.5kg

- Prematurity (<37 wks) - ↑ mean gestational age from 8.3% to 12.7% - 25% ↓ risk for <37 w - Cesarean section rate - ↓ CS rate from 42.6% to 54.8% - 13% ↓ risk for CS -Mean maternal age from 31.1 y to 32.7 y - ↓ mean maternal age

-29.2 y vs 32.4 ( of Greeks)

-

Conclusions-2

• Greece: • Migrants: • Maternal age ≥30 → independent • Maternal age at gestation: risk factor: effect modifier - low birth weight acts synergistically with - prematurity “healthy immigrant effect” - CS • Period 2012-2014 → independent • For maternal ages >35 years→ risk factor: associations not statistically - low birth weight significant → - CS possibly long-term immigrants • Low birth weight → independent residing in Greece? risk factor: “ effect” - CS

Issues to be considered

• Migrants from countries with low HDI do not differ from Greeks concerning perinatal parameters, probably due to very bad socioeconomic conditions, or their very small number

• From our sample a certain percentage are long term immigrants in Greece

• Economic crisis had an impact on Greek standards of living and probably on long-term immigrants too

• The “Healthy Immigrant Paradox” could have been more pronounced before the economic crisis Overall Conclusion

• In total immigrant women deliver: - at an earlier age (< 35 years) - vaginally - babies with higher birth weights - more mature babies ↓ thus present more favorable birth outcomes and prove ↓ “Healthy Immigrant Paradox”

Despite its current difficulties… Greece is a most beautiful country, deserving your visit! Thank you!