Features of breast cancer in developing countries, examples from North-Africa

European Journal of Cancer (2014) xxx, xxx– xxx

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Features of breast cancer in developing countries, examples from North-Africa Marilys Corbex a,⇑, Sabiha Bouzbid b, Paolo Boffetta c,d a

Institute of Tropical Medicine, Nationalestraat, 155, 2000 Antwerpen, Belgium Badji Mokhtar University, Faculty of Medicine, Annaba, Algeria c Institute for Translational Epidemiology and Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY, United States d International Prevention Research Institute, Lyon, France b

Received 24 October 2013; received in revised form 10 March 2014; accepted 14 March 2014

KEYWORDS Epidemiology Breast cancer Developing countries North-Africa Male breast cancer Inflammatory breast cancer Triple negative breast cancer

Abstract Epidemiological features of breast cancer appear to be different in developing countries compared to Western countries, with notably large proportions of young patients, male patients and aggressive forms of the disease. Using North-Africa (Morocco, Algeria, Tunisia, Libya and Egypt) as an example, we document the magnitude and explore possible explanations for such patterns. Articles and reports published since the seventies were reviewed. Results show that breast cancer incidence in females is 2–4 times lower in North-Africa than in Western countries while incidence in males is similar. Consequently, the relative proportion of male breast cancer is high (2% of all breast cancers). Similarly, the incidence of aggressive forms of the disease, like inflammatory or triple negative breast cancer (in females), is not higher in North Africa than in Western countries, but their relative proportion in case series (up to 10% for inflammatory and 15–25% for triple negative) is significantly higher because of low incidence of other forms of the disease. In North Africa, the incidence among women aged 15–49 is lower than in Western countries, but the very low incidence among women aged more than 50, combined to the young age pyramid of North-Africa, makes the relative proportions of young patients substantially higher (50–60% versus 20% in France). Such epidemiological features result mainly from peculiar risk factor profiles, which are typical for many developing countries and include notably rapid changes in reproductive behaviours. These features have important implications for breast cancer control and treatment. Ó 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author: Tel.: +32 484211515; fax: +32 32476258.

E-mail addresses: [email protected], [email protected] (M. Corbex). http://dx.doi.org/10.1016/j.ejca.2014.03.016 0959-8049/Ó 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Corbex M. et al., Features of breast cancer in developing countries, examples from North-Africa, Eur J Cancer (2014), http://dx.doi.org/10.1016/j.ejca.2014.03.016

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Text concluding boxes In North Africa compared to Western countries, – the incidence of breast cancer is:  lower among females (approximately 1.5–2 times lower among females aged less than 50, and 3–4 times lower among females aged more than 50).  similar among males, but its relative frequency is higher because of low incidence of female breast cancer. – the relative frequency of triple negative and inflammatory breast cancer is also higher.

1. Introduction Breast cancer (BC) incidence is rising all over the world, especially in developing countries [1]. BC is now the most common cancer among both sexes in the less developed regions of the world [2], while in 2002 it was the fourth [3]. In many countries, this rise has made BC an increasingly important public health issue. In developing countries BC presents epidemiological features which differ from those observed in Western countries: age at onset is younger and it has been reported that the disease is more aggressive and some rare forms of BC more frequent (inflammatory breast cancer or male breast cancer for example) [4–7]. However, these peculiar features have not been thoroughly explored to date and their underlying causes raise questions among clinicians. Here we aim to describe these peculiar features rigorously, using the example of North-Africa, a developing region that includes five countries (Morocco, Algeria, Tunisia, Libya and Egypt). We also aim to clarify the possible underlying causes of these features. The scarcity of published data, typical of developing regions, required a special review effort. Many reports / thesis /presentations at meetings were reviewed. A decade of work in the region enabled the authors to access and analyse most of the information available. Findings are presented here for the first time in a comprehensive way, and compared with similar information for two Western countries (i.e. France and the USA). This comparison enlightens the peculiar features of BC in a developing region. 2. Methods Documents providing original data on BC in North Africa were collected throughout the years. Registry reports, unpublished data, private notes and personal correspondence were included, and the following sources were searched without restriction on the dates:

Medline, Embase, Scopus, Biological Abstracts, Popline and African Journals OnLine. Search terms used include breast cancer/neoplasm and the truncated names of countries/populations (e.g. ‘Egypt*’). Documents in English and French were reviewed. No selection on study design was carried out. The crude incidence and age standardised incidence rates (ASRs) presented are reported from Cancer incidence in Five continents (CI-5) Volume IX for Central Tunisia and volume X for Gharbeia (Egypt), Se´tif (Algeria), Benghazi (Libya), France and USA [8,9], and directly from the registries reports or publications for Annaba [10] (Algeria), Casablanca [11,12] and Rabat [13] (Morocco), North Tunisia [14–16] (with more recent data than in CI-5 X) and Sfax (South Tunisia) [17,18]. Confidence intervals (CIs) of ASR were calculated according to Jensen et al. [19]. To estimate incidence of sub-types of BC (inflammatory BC, triple negative BC) simple cross-multiplications were used. 3. Results and discussion 3.1. Prevalence of BC risk factors BC risk factors are well characterised, the major ones are presented in Table 1. Few North-African casecontrol studies have investigated the aetiology of BC [20–22] and have reported, as expected, the same risk factors as studies carried out in Western countries. The predominant hormonal model proposed for causation of BC implies that the risk factors intervening in the aetiology of BC are similar across regions of the world [23]. However the prevalence of these risk factors can vary remarkably from one region to the other. The number of children, the age at first child, the duration of breastfeeding, the age at menopause, the prevalence of hormonal replacement therapy and alcohol consumption all differ significantly between North-Africa and Western countries (see Table 1). They define a risk profile that is more protective in North-Africa than in Western countries, and that is expected to impact significantly on incidence. Variations with time are also important to consider: in North Africa reproductive behaviours have changed rapidly drifting from low-risk profiles, i.e. many children, young age at first pregnancy, long duration of breastfeeding, etc. (see Table 1). For example in Egypt, total fertility rates were 6.0 children per women in 1988 [24] compared to 3.1 in 2008 [25] and in Morocco, 5.7 in 1980 [26] compared to 2.5 in 2003 [27]. As a result, risk profiles are more protective in older North African women than in younger ones. 3.2. Prevalence of screening Recently, pilot mammography screening initiatives have been carried out by governments in Morocco,

Please cite this article in press as: Corbex M. et al., Features of breast cancer in developing countries, examples from North-Africa, Eur J Cancer (2014), http://dx.doi.org/10.1016/j.ejca.2014.03.016

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Table 1 Risk factors of breast cancer and their prevalence in North-Africa and Western countries, recently and in the eighties/seventies. Risk factors*

Effect on risk of breast cancer (BC)

Prevalence in Egypt/Morocco and France/USA

Familial history %

Risk increased by 80% if one first degree relative is affected, by 193% if two [70]

Number of children &

Risk reduced by 16% for every two births [71]

Age at first child %

Risk increased by 40% for first birth after age 35 versus before age 20 [71]

Breast feeding &

Risk reduced by 4.3% for every 12 months of breastfeeding [76]

Age at menarche &

Risk reduced by 7% for each year menarche is delayed [81]

Age at menopause %

Risk increased by 3% for each year menopause is delayed [87]

Oral contraceptive %

Risk increased by 24% among current users [91]

Hormone replacement therapy %

Risk increased by 35% among current users [87]

Alcohol %

Risk increased by 32% for an intake of 35– 44 g alcohol/day [97]

Body mass index %

Risk of post-menopausal cancer increased by 50% in overweight women [99]

In Western countries approximately 13% of BC patients report familial history among first degree relatives in [70] North-Africa.: No data are available Mean number of children: – USA [72]: 1.9 (2011) 1.8 (1980) – France [72]: 2.0 (2011) 1.9 (1980) – Egypt: 3.1 (2008) [25] 6.0 (1988) [24] – Morocco: 2.5 (2004) [27] 5.7 (1980) [26] Mean age at first child: – USA: 24 (2010) [73] 2 (1980) [74] – France: 28 [75] (2010) 25 (1980) – Egypt: 22 (2008) [25] 21 (1988) [24] – Morocco: 23 (2004) [27] 21 (1987) [26] Mean duration of breastfeeding: – USA (babies breastfed at least 6 months): 24% (1980) [78] 42% (2008) [77] – France: 2.3 months (2008) [79] 3.4 months (1980) [80] – Egypt: 17.7 months (2008) [25] 17.3 months (1988) [24] – Morocco: 14.2 (2004) [27] 14.4 months (1987) [26] Mean age at menarche – USA: 12.3 (2002) [82] 12.7 (1963–70) [83] – France: 12.8 (2006) [84] 13 (1979) [85] – Egypt: 12 (2007)[41] – – Morocco: 13.7 (1991) [86] 13.2 (1982) [86] Mean age at menopause – USA: 52.5 (2007) [88] 51.3 (1998) [85] – France: 52 (1995) [89] 52 (1980) [85] – Egypt: 46 (1999) [40] – Morocco: 45 (1993) [90] Prevalence of oral contraceptive (current users): – USA: 17% (2010) [92] 15% (1985) [93] – France [94]: 42% (2010) 28% (1978) – Egypt: 9% (2008) [25] 15% (1988) [24] – Morocco: 40% (2004) [27] 23% (1987) [26] Prevalence of HRT: – USA [93] (current users): >20% (2002) – France [93] (current users): 9–16% (2003) – Egypt [95] (ever user) <10% (2006) – Morocco [96] (current users): 5% (2002) Alcohol consumption among adult women [98] – USA: 38% last year abstainers (2002) – France: 9% last year abstainers (1999) – Egypt: 98% last year abstainers (2001) – Morocco: 99% women are life long abstainers (2003) Prevalence of overweight or obese women (above age 15) [100] – USA: 70% (2006) 42% (1980) – France: 41% (2007) 27% (1981) – Egypt: 74% (2008) 57% (1992) – Morocco: 55% (2004) 33% (1992)

*

Significant breast cancer risk factors such as breast density, BRCA1/2 mutations or radiation exposure are not included because adequate data about their prevalence in North Africa are missing.

Algeria, Tunisia and Egypt, but they have covered only a very small fraction of women in these countries [28–30]. The largest programme took place in Egypt: 21,000 women were screened in 2008, which represented 0.25% of the eligible population (women above 45 years) [31]. Screening based on individual initiative is rare and

concerns almost exclusively women from the high socio-economic class. A World Health Organisation (WHO) study conducted in 2003 on a large representative sample of the Moroccan population revealed that only 2.1% of the women above 40 had ever had a screening mammogram in their life [32]. In Egypt, a

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similar study conducted by United States Agency for International Development (USAID) revealed that only 1.7% women above 40 had a mammogram within the past 12 months (unpublished results from the Egypt Demographic and Health Survey (EDHS) 2008 [25]). 3.3. Incidence in North-Africa compared to France and USA Cancer registries have developed recently in Morocco (2007) and Libya (2006), while others existed since the 1990s in Algeria, Tunisia and since 2002 in Egypt. Their data quality has been considered as ‘good or acceptable’ by experts [33]. Are included here the North African registries we consider to have ‘acceptable’ data quality, based on our collaboration with them and careful review of their data (registries from Casablanca, Rabat, Annaba, Setif, Sfax, North Tunisia, Central Tunisia, Benghazi and Gharbeia, see map on Fig. 1). The registries of Setif, North Tunisia, Central Tunisia, Benghazi and Gharbeia are included in Cancer Incidence in Five Continents (CI-5) volume IX and/or X [8,9]. Crude and agestandardised incidence is displayed in Table 2, together

with incidence from France and USA for comparison purposes. In North-Africa, BC is the most common cancer among women, representing 25% to 35% of all female cancers (see Table 2). With a crude incidence ranging between 16/100,000 inhabitants (in Benghazi, Libya) and 39/100,000 inhabitants (in Rabat, Morocco), the incidence of BC in North-African countries is 4–9 times lower than in France (see Table 2). If North-African countries had the same age pyramid as France, their incidence rates would still be 2–4 times lower (see ASR in Table 2). This difference is attributable to various factors and primarily to the low prevalence of the major risk factors of BC in North-African countries, a situation typical of developing countries. As illustrated in Table 1, the distribution of risk factors in North-Africa has not yet matched that observed in Western countries. Variations in risk factor prevalence can affect incidences very significantly [34,35]. The presence of wide scale screening in Western countries and its absence in North Africa may also explain a substantial part of the incidence difference, notably in women above 50 (the target group for organised screening programmes in Europe).

Fig. 1. Map of the North African registries presented and corresponding age standardised incidence rate (ASR) for female breast cancer.

Table 2 Incidence of female breast cancer from selected population-based registries in North-Africa. Country (total population in millions)

Registry area (population covered in millions)

Years covered

Crude incidence

Age standardised incidence rate (ASR) [confidence interval (CI)]

% of female cancers

Morocco (32.6)

Casablanca [12] (3.6) Rabat [13] (1.26) Se´tif [9] (2.2) Annaba [10] (0.60) Sfax [18] (0.84) North Tunisia [16] (4.8) Central Tunisia [8] (0.8) Benghazi [9] (1.6) Gharbia Governorate [9] (5.0) 11 districts [9] (6.7) 18 states (SEER) [9] (7.0) 18 states (SEER) [9] (37.5)

2005–2007 2005 2003–2007 2007–2009 2000–2002 2004–2006 1998–2002 2003–2005 2003–2007 2003–2007 2003–2007 2003–2007

37.5 38.8 20.5 35.2 25.2 32.3 25.2 16.0 37.8 154 100 134

36.4 [34.8–38.0] 35.8 [29.5–42.1] 29.8 [27.5–32.0] 34.1 [30.3–37.9] 28.0* 31.8 [30.7–33.3] 29.8 [26.5–33.1] 22.9 [20.4–25.4] 45.4 [43.9–46.9] 97.5 [96.4–98.6] 83.9 [82.8–85.0] 88.8 [88.4–89.2]

34 33 30 47 31 34 31 23 39 35 30 29

Algeria (37.9) Tunisia (10.7)

Libya (5.6) Egypt (83.7) France (65.8) USA black (38.9) USA white (223.5)

* Confidence interval could not be calculated because the underlying population age-distributions used for incidence calculations were not fully documented in the registry report.

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It has been suggested that screening may increase breast cancer incidence by up to 30% where organised programmes take place [36]. Underreporting and underdiagnosis (women not diagnosed at all) are not likely to bias significantly incidence in North Africa, as we explained recently elsewhere [37].

Rabat registry which is 100% urban and of relatively high socio-economic status [43] has a higher incidence (ASR = 35.8) than the populations covered by the Sfax registry (ASR = 28.0) which is only 64% urban [18].

3.4. Incidence variations within neighbouring countries

Assessing time trends in incidence of BC in North-Africa is difficult due to the scarcity of long-term registry data, only data from Tunisia and Algeria are available for a sufficiently long time. The Algerian Se´tif registry reports indicate that the ASR of BC more than doubled in 20 years, from 10.4 in 1986–1989 to 24.8 in 2006–2008 [9]. The Northern Tunisia registry reports indicate that the ASRs increased from 23.9 in 1995– 1996 to 30.2 in 2002–2003 [14,16]. In the period 1993– 2006 the central Tunisia registry reports an annual percent change of +2.2% [44]. Interestingly, such an increase is higher than the one observed in France in 1990–1999 (1.2% per year) before screening was implemented [45]. Given the very low coverage of screening in North-Africa, its effect on time-trends is expected to be negligible.

3.5. Time trends in incidence

With ASR of 22.9 or 28.0 (Table 2), Benghazi (Libya) and Sfax (Tunisia) appear to have a much lower incidence than Gharbeia (Egypt) (ASR = 45.4) (see Fig. 1). Such differences may be partly attributable to differences in quality and completeness of registration, but differences in risk factor prevalence among populations covered by the registries are also likely to play a role. We wish here to raise to the reader’s attention about the socio-economic and education levels of populations as these can critically affect reproductive factors, which in turn affect BC incidence. It has been shown that the incidence of BC correlates positively with socio-economic status [38,39]. North-African countries, like most developing countries, have tremendously heterogeneous populations in terms of socio-economic level with notably large differences between urban and rural populations. For example, in Egypt between urban governorates of the North and rural governorates of the South, the fertility rate varies from 2.5 to 3.9 and the age at first birth from 24.3 to 20.4 years [25]. Rural women reach menopause earlier than urban women (on average 6 years earlier according to a study conducted in Egypt [40]) and mean age at menarche varies also significantly according to socio-economic status [41]. A study conducted by the Egyptian cancer registry revealed that BC incidence rates were two to three times lower in rural women than in urban women [42]. This suggests that the urban/rural composition of the districts covered by the registries may contribute to substantial part of the differences observed in Table 2. For example, the population covered by the

3.6. Age specific incidence Contrary to what is observed in Western countries, in North-Africa BC appears to be predominantly a disease of young women. As illustrated in Fig. 2 for Egypt and Morocco, the incidence of BC is higher in women 45–49 than in women 65–69. The curves are similar for the other North-African countries (data not shown). These age distributions combined with the young age pyramid of North-African countries, result in case series where 50% to 60% of patients are below 50 years of age, while in case series from the USA or France this proportion is around 20%. This large proportion of young patients creates the misleading notion that ‘BC affects women at a younger age than in Western countries’ [4,46].

500 400

Gharbeia

inc idenc e per 100,000

Casablanca

300

France USA

200 100

4

+ 85

4

9 -7

-8 80

75

4

9 -6

-7 70

65

9 -5

9

4 -5

-6 60

55

50

9

4 -4

-4 45

40

4 -3

4

9 -2

-3 35

30

25

-2

-1 15

20

9

0

Fig. 2. Age specific incidence of female breast cancer in Morocco, Egypt, France and United States of America (USA). Sources: population based registries of Casablanca [12] (Morocco), Gharbeia [9] (Egypt), France [9] (11 departmental registries) and USA [9] (18 SEER registries).

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However, as shown in Fig. 2 the incidence of BC among women below 40 in North-Africa is similar to that in France or USA and the incidence among women 40– 50 is lower. Furthermore the ASR for women 15–49 in the four North African CI-V X registries (Setif-Algeria, Lybia, Northern Tunisia and Egypt) is 31/100,000, compared to 61/100,000 in France [9]. This indicates that young women in North-Africa are not at increased risk of BC compared to their Western counterparts. What is striking is that among women above 50, the incidence is considerably lower in North-Africa than in France or the USA (ASR50+ is 104/100,000 in the four North African CI-V X registries compared to 340/100,000 in France [9]) (see also Fig. 2). This difference reflects a cohort effect: In North-Africa women currently in their 70s have a much more favourable risk profile than women in their 40s: they gave birth to more children, had them much earlier, and breast fed them for a longer time [24–27]. It is interesting to note that such a cohort effect is also visible for the USA and France, 25 years and 10 years respectively before North-Africa (Fig. 2). Mass screening of women above 50 years of age in USA and France also contribute to widen the gap with North Africa. 3.7. Incidence of breast cancer in men Male BC is a rare disease and is associated with strong genetic susceptibility; some environmental risk factors, including obesity, testicular disorder, radiation exposure and exposure to exogenous oestrogen, have also been shown to increase risk (for review see Ruddy and Winer, 2013) [47]. In the USA, it has been established that ASR of BC is slightly higher among Black men than among White men but the reasons for this difference remain unknown [48]. Across Caucasian populations in Europe and America, ASR are uniform around 0.8/100,000 [8,9]. In North-Africa, male BC appears to clinicians to be more frequent than in Europe or the USA, and various causes, including genetic ones, have been invoked to

explain this higher frequency [49]. Table 3 shows that indeed, the percentage of male BC among all BC is higher in North-Africa (Egypt: 1.6% of all BC, Algeria: 2.8%, etc.) than in France (0.8%) or US whites (0.7%), but this is due to the relatively low incidence of female BC and not to a higher incidence of male BC. Indeed, the ASRs of male BC in North-African countries are all below 0.9 and do not differ significantly from ASR in France or US White males (see CI in Table 3). Male BC ASR varies also across North-African country, but not significantly (see CI in Table 3), such differences are attributable to random sampling variations, issues in completeness of registration may also contribute. 3.8. Aggressive forms of female BC In many publications it is reported that BC is more aggressive in North Africa than in Western countries, the reason for this remaining unclear [4–7,50,51]. It is well established that BC aggressiveness decreases with age of onset [52], so one can argue that the majority of patients in North Africa being young, the proportion of aggressive BC in cases series is de facto expected to be high. However the issue is probably more complex; to better explore it, we reviewed the data of two aggressive forms of BC that have been reported as frequent in North Africa: inflammatory breast cancer (IBC) and triple-negative BC [4,6,50]. 3.8.1. Inflammatory breast cancer IBC is a particularly aggressive form of BC characterised by inflammatory signs and bad prognosis [53]. In the USA, IBC represents not more than 2% of all BC and IBC cases are significantly younger than non-IBC cases [54]. IBC incidence is also significantly higher among black women (3.1/100,000) than among white women (2.2/100,000) [54]. No population-based data on IBC is available from North-Africa; only proportions of IBC in cases series have been published and the challenging definition of the disease (IBC can be confused with locally advanced

Table 3 Incidence of male breast cancer from selected population-based registries in North-Africa. Country

Registry area [reference]

Number of registered male breast cancer (BC)

Age standardised incidence rate (ASR) [confidence interval (CI)]

% of male BC among all BC

Morocco

Casablanca district [12] Rabat [13] Se´tif district [9] Northern Tunisia [9] Central Tunisia [8] Benghazi [9] Gharbia Governorate [9] 11 districts [9] 18 states (SEER) [9] 18 states (SEER) [9]

10 3 12 45 8 6 58 276 246 1675

0.5 [0.1–0.9] 1 [0.0–2.2] 0.6 [0.3–0.9] 0.6 [0.4–0.8] 0.9 [0.3–1.5] 0.5 [0.1–0.9] 0.8 [0.6–1.0] 0.8 [0.70–0.90] 1.1 [0.96–1.24] 0.7 [0.66–0.74]

1.5 2.3 2.8 2.0 2.5 1.6 1.6 0.8 0.9 0.8

Algeria Tunisia Libya Egypt France USA black USA white

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BCs) makes them difficult to compare. Historically, very high proportions of IBC were reported, up to 59% in Tunisian cases series [6,55] or up to 65% in Egyptian ones [56] in the seventies. A review of all the Tunisian studies performed since the seventies revealed a trend of decreasing incidence in IBC diagnoses from 50% in the seventies to less than 10% nowadays. This decline was attributed to the use of more stringent criteria for IBC diagnosis, the trend to earlier diagnosis and the country’s increasing socioeconomic level [57]. In 2005, we reviewed inflammatory status from the total 2003– 2004 cases series (N = 1936) treated at the oncology departments of Blida, Annaba (Algeria) and Casablanca (Morocco). The percentage of IBC was homogeneous across centres and reached 10% using a non-stringent definition of the disease (data not shown). In Egypt too, recent studies display proportions of IBC around or below 10% [58]. Using the BC incidence presented in Table 2, it is possible to approximate that if IBC cases represent 10% of the patients in North-African series, then IBC incidence should lie between 2 and 4/ 100,000, which is not notably different from what is observed in the USA. It would mean that it is the relatively low incidence of non-IBC patients that makes IBC five times more frequent in North-African case series and not a genuinely higher incidence of IBC (reasoning comparable to the one we made for male BC). 3.8.2. Triple negative breast cancer Triple-negative BC is defined as BC that is negative for oestrogen receptor, progesterone receptor and human epidermal growth factor receptor 2. Triple negative tumours are aggressive and have poor survival [59]. Studies performed in developing countries, in large unselected BC samples report a high proportion of triple negative BC, for example 55% in Senegal/Nigeria [60], 39% in Saudi Arabia [61], 29% in Malaysia [62] or 23% in China [63]. Such proportions are higher than those observed in White populations of Europe and North America, where the proportion of triple negative BC is around 10–12% [64,65]. Table 4 displays the proportions of triple-negative BC documented in large cases series from North-Africa, they are relatively high and vary from 17% to 28%. Recent studies show that the risk factors differ to some degree between triple-negative BC and other forms

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of the disease (for review see [59]). Triple negative BC is associated with young age, high parity, short/absent breastfeeding, obesity/over-weight before menopause and BRCA1 mutations. The increased risk conferred by young age and high parity may explain, at least in part, the relatively high proportion of triple-negative cases observed in Northern African and other developing countries. But as shown in previous paragraphs, high proportions do not mean high incidence. If we apply the same reasoning than for IBC, and assume a proportion of triple negative around 20% in North-African cases-series (the mean of studies reported in Table 4), the incidence should then lie between 4 and 8/100,000, which is much lower than the incidence observed in the USA (28/100,000) [66] and near the one reported recently for Malaysia (6/100,000) [62]. Interestingly in the Malaysian study, where three ethnic/cultural groups at different level of socio-economic transition were compared, the proportion of triple-negative cases was significantly higher in the group with the most traditional life-style (37%) compared to the most ‘Westernized’ group (23%) but the incidence was lower (3.6/ 100,000 compared to 8.1/100,000) [62]. The relation between IBC and triple negative status has not been much studied. A study performed in Algeria on 117 IBC and 59 non-IBC revealed that the proportion of triple negative was similar in both groups, around 18% [67], suggesting that mechanisms of aggressiveness in IBC are different from those that are captured by receptor status. To conclude on aggressive forms of BC, it appears clearly that the proportions of IBC or triple-negative BC are higher in Northern African case-series than in Western ones, even if incidence is not higher. This has to be taken into account when planning treatment and palliative care resources. 4. Conclusion In North-Africa, BC displays specific features including young age at diagnosis, high proportion of aggressive BC and high proportion of male BC. These features stem mainly from risk factor profiles that are different from those observed in Western countries, and which result in much less post-menopaused women being affected with BC. These risk factor profiles result from rapid changes in reproductive habits and are

Table 4 Proportion of triple negative breast cancers in selected cases series from North-Africa. Reference

Fourati et al. (2012) [101]

Rais et al. (2012) [102]

Bennis et al. (2012) [103]

El-Hawary et al. (2012) [104]

Salhia et al. (2011) [105]

Place Case series Triple-negative [95% confidence interval (CI)]*

Tunis, Tunisia 966 cases (2007–2009) 23% [19–26%]

Rabat, Morocco 918 cases (2007–2008) 17% [14–19%]

Fez, Morocco 366 cases (2007–2010) 17% [13–22%]

Mansoura, Egypt 274 cases (2008–2010) 28% [23–34%]

Cairo and Minia, Egypt 198 cases (no dates) 19% [13–25%]

*

95% CI were not available in the original articles but were calculated from the data published.

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common to many developing countries. Thus the features of BC observed in North Africa are likely to be observed in other regions of the world. Risk factor profiles in North Africa and other developing regions will continue to evolve and presumably reach the one observed in Western countries today, however this may take a few more decades depending on the rapidity of societal changes in each country. In the mean time, countries have to plan resources for BC early detection, treatment and palliative care accordingly: The large proportion of young cases advocates against the sole use of mammography screening to ensure early detection, since in women less than 50 this approach has been suggested to cause more harm than benefit [68,69]. The relatively high frequency of the aggressive form of the disease, which necessitates costly chemotherapy treatments, needs to be considered when planning treatment/health insurances resources.

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Conflict of interest statement None declared.

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