Pine Nuts: A Review of Recent Sanitary Conditions and Market Development

Abstract

Pine nuts are non-wood forest products (NWFP) with a constantly growing market notwithstanding a series of phytosanitary issues and related trade problems. The aim of this paper is to review the literature on the relationship between phytosanitary problems and trade development. Production and trade of pine nuts in Mediterranean Europe have been negatively affected by the spreading of Diplodia sapinea (a fungus) associated with an adventive insect Leptoglossus occidentalis (fungal vector), with impacts on forest management, production and profitability and thus in value chain organization. Reduced availability of domestic production in markets with a growing demand has stimulated the import of pine nuts. China has become a leading exporter of pine nuts, but its export is affected by a symptom caused by the nuts of some pine species: ‘pine nut syndrome’ (PNS). Most of the studies mentioned in the literature review concern PNS occurrence associated with the nuts of Pinus armandii. We highlight the need for a comprehensive and interdisciplinary approach to the analysis of the pine nuts value chain organization, where research on food properties and clinical toxicology may be connected to breeding and forest management, forest pathology and entomology, and trade development.

Full text

Article
Pine Nuts: A Review of Recent Sanitary Conditions
and Market Development
Hafiz Umair Masood Awan 1ID and Davide Pettenella 2,*ID
1Department of Forest Science, University of Helsinki, FI 00014 Helsinki, Finland;
awan48@gmail.com or hafiz.awan@helsinki.fi
2
Department Land, Environment, Agriculture and Forestry, University of Padova, 35020 Legnaro (PD), Italy
*Correspondence: davide.pettenella@unipd.it; Tel.: +39-049-827-2741
Received: 16 July 2017; Accepted: 14 September 2017; Published: 27 September 2017
Abstract:
Pine nuts are non-wood forest products (NWFP) with a constantly growing market
notwithstanding a series of phytosanitary issues and related trade problems. The aim of this paper is
to review the literature on the relationship between phytosanitary problems and trade development.
Production and trade of pine nuts in Mediterranean Europe have been negatively affected by the
spreading of Diplodia sapinea (a fungus) associated with an adventive insect Leptoglossus occidentalis
(fungal vector), with impacts on forest management, production and profitability and thus in value
chain organization. Reduced availability of domestic production in markets with a growing demand
has stimulated the import of pine nuts. China has become a leading exporter of pine nuts, but its
export is affected by a symptom caused by the nuts of some pine species: ‘pine nut syndrome’ (PNS).
Most of the studies mentioned in the literature review concern PNS occurrence associated with the
nuts of Pinus armandii. We highlight the need for a comprehensive and interdisciplinary approach to
the analysis of the pine nuts value chain organization, where research on food properties and clinical
toxicology may be connected to breeding and forest management, forest pathology and entomology,
and trade development.
Keywords:
pine nut; pine nut syndrome (PNS); pine mouth syndrome (PMS); cacogeusia; non-wood
forest products; Leptoglossus occidentalis (Western conifer seed bug); Diplodia sapinea (Sphaeropsis blight)
1. Introduction
There is a great variety of species in the genus Pinus that produce nuts of commercial interest.
This variety is connected to tree productivity, nutritional and medicinal value, taste and textural
properties, and commercial value of the nuts. Despite these variations, when retailed, they are all
included under the generic name ‘pine nuts’ [1].
This paper reviews the recent literature on pine nuts from an interdisciplinary perspective.
The motivations for our survey are due to the remarkable development of the international pine
nuts market; a development based more on empirical evidence than on systematic and clear results
deriving from production and trade data recorded by statistical institutions. For these reasons, we try
to highlight the growing role played by this category of products in the global market, with a focus on
the European Union (EU) market which has seen the most radical changes in its structure, and the
main issues considered by the scientific literature, i.e., pine forest phytosanitary problems and human
health problems connected to the consumption of some species of pine nuts.
The paper is structured as follows: the introductory section highlights the historical origins
of pines and some general aspects of the pine nut sector, such as the nutritious and dietary values.
Details of the research methodology in the description of market development and literature review
follow. We then present the results of this combined analysis: the production and trade patterns at the
Forests 2017,8, 367; doi:10.3390/f8100367 www.mdpi.com/journal/forests

Forests 2017,8, 367 2 of 17
world and EU level and the current issues that hamper market development, making reference to pine
nut syndrome (PNS), pathogenic fungi like Diplodia sapinea (Fr.) Fuckel [
2
,
3
] or Sphaeropsis blight and
the related pest Leptoglossus occidentalis Heidemann (the western conifer seed bug). Lastly, conclusions
and suggestions are made for further research.
2. Pines and Pine Nuts: General Aspects
It is thought that the first pines emerged somewhere in northern Asia around 180 million
years ago. Geologically, it was the Triassic Period in the Mesozoic Era (age of reptiles) [
4
–
6
].
Pines gradually differentiated into Haploxylon (soft or white) pines and Diploxylon (hard or yellow)
pines [
7
] (pp. 51–52) about 75 million years ago [
4
]. Today, these two distinct sub-genera are still
considered to be in the world’s flora classification [
4
] (see [
4
,
6
] for further historical and cultural
details). They are both important sources of seeds for human consumption. Humans started to utilize
pine nuts in the Paleolithic era [
8
]; the Food and Agriculture Organization reported the utilization
of pine nuts as a comestible food item starting from pre-historic times [
9
,
10
]. Today’s busy lifestyles
provide an opportunity to use tree nuts as they are nutritious, handy and tasty snacks, and pine nuts
are used in traditional recipes in many countries.
The pine nut species that are consumed domestically may differ from those that have
an important commercial role and are traded [
11
,
12
]. For instance, Pinus armandii Franch. (Chinese white
pine), Pinus tabuliformis Carr (Chinese red pine), Pinus yunnanensis Franch (Yunnan Pine),
and Pinus massoniana
Lamb (Masson’s pine) are mainly imported into Europe from China and differ
from the domestically produced Pinus pinea L. nuts [
13
] (p. 2), [
14
]. A reliable online working list of
all plant species currently contains 636 scientific species records for the genus Pinus [
15
]. Of these
636 records, 126 are accepted species names. Of these 126 species of Pinus that exist worldwide, only 29
provide edible nuts according to the Food and Agriculture Organization [
9
], while 20 are traded locally
or internationally. The species that are commercially important for providing pine nuts are listed
in Table 1.
Table 1. Comestible species of pine nuts in the world.
Species Natural Range Remarks
Soft Pines (Haploxylon)
P. ayacahuite Engelm. ex Schltfl. Central America, Mexico Traditional food for indigenous tribes
P. albicaulis Engelm United States and Western Canada Traditional food for indigenous tribes
P. cembra L. Europe (Alps and Carpathian Mountains) Locally important
P. flexilis E.James United States and Western Canada Traditional food for indigenous tribes
P. gerardiana Wall. ex D.Don Pakistan, East Afghanistan, North India Important in international trade
P. koraiensis Siebold & Zucc. East China, Japan, Korea, South-east Siberia Important in international trade
P. lambertiana Douglas Western United States (California, Oregon) Traditional food for indigenous tribes
P. monticola Douglas ex D.Don North-west United States and adjoining Canada Traditional food for indigenous tribes
P. pumila (Pall.) Regel East Siberia, East China, Japan, Korea Locally important
P. sibirica Du Tour Mongolia, Russia (Central Siberia) Nuts are ground into cooking oil
P. strobiformis Engelm North Mexico, South-west United States Traditional food for indigenous tribes
Pinon pines North Mexico, South-west United States A complex group of about 13 species.
Many are important food sources
Hard Pines (Diploxylon)
P. coulteri D.Don California (United States) Traditional food for indigenous tribes
P. pinea L. Mediterranean Europe and Near East Important in international trade
P. ponderosa Douglas ex C.Lawson United States and Western Canada Traditional food for indigenous tribes
P. sabiniana Douglas ex D.Don California (United States) Traditional food for indigenous tribes
P. roxburghii Sarg. India, Pakistan Traditional food source
P. torreyana Parry ex Carr. California (United States) Traditional food for indigenous tribes
Source: FAO [16] and Ciesla [9].
Of these 20 species, only three are of much international significance: P. koraiensis from China,
P. pinea from southern Europe, P. gerardiana from Pakistan and Afghanistan [
16
,
17
]. Handy et al. [
18
]
mentioned Pinus edulis Engelm, P. monophylla Torr and Frém, P. pumila (Pallas) Regel, P. sibirica,

Forests 2017,8, 367 3 of 17
P. wallichiana A. B. Jacks, P. tabuliformis Carr., P. yunnanensis Franch., P. gerardiana,P. koraiensis,
P. massoniana Lamb, as the most relevant species exported worldwide. Other species are usually
sold in local markets where they originate [10].
Pine nuts are popular in different parts of the world, especially in the Mediterranean, Middle East,
Asia, and in the southwestern United States by Native Americans [
19
] (p. 285). The majority of ecological
and silvicultural research has been focused on P. pinea [
8
,
20
–
22
]. It has been stated that in some rain-fed
areas (i.e., Mediterranean areas) gathering of cones containing pine nuts yields a much better income
in a short period than harvesting wood after long rotations [22].
Tree nuts can be defined as “dry fruits with generally one seed in which the overall wall becomes
hard at maturity” [
23
]. However, a pine nut is not a true nut because it lacks an outer carpel (though it is
a tree nut). They are instead edible small-sized ivory-coloured nutritious seeds [
10
,
17
,
19
,
24
], which are
collected from the cones of different pine species [24,25] and are oil rich [13].
The kernels of European stone pine (P. pinea), which is indigenous to the Mediterranean area,
are sometimes described as Mediterranean pine [
26
] or Italian pine nuts. In Neo-Latin languages,
pine nuts are known as pinoli or piñone (in the US they are often called pignoli). In the other parts of the
world, kernels of the pinyon pines (P. edulis and P. monophylla), which grow in the southwestern US
and in northern Mexico, are known as pinon nuts [25].
Pine nuts are a source of valuable nutrients (Table 2). P. pinea supplies double the amount of
protein than Chinese (P. koraiensis) and Pakistani pine nuts (P. gerardiana) [
27
]. However, the latter
two species provide more carbohydrate and fats, which are very important components of our diet.
Pakistani pine nuts in particular are a potentially rich source of the carbohydrates that may be the
most useful for athletes.
Table 2. Nutrient values and weights for edible portion of pine nuts.
Nutrient Unit Value Per 100 g 1 Cup (135 g) 1 oz (167 Kernels)
or (28.35 g) 10 Nuts (1.7 g)
Proximates
Water g 2.28 3.08 0.65 0.04
Energy kcal 673 909 191 11
Protein g 13.69 18.48 3.88 0.23
Total lipids (fat) g 68.37 92.3 19.38 1.16
Carbohydrate, by difference g 13.08 17.66 3.71 0.22
Fiber, total dietary g 3.7 5 1 0.1
Sugars, total g 3.59 4.85 1.02 0.06
Minerals
Calcium, Ca mg 16 22 5 0
Iron, Fe mg 5.53 7.47 1.57 0.09
Magnesium, Mg mg 251 339 71 4
Phosphorus, P mg 575 776 163 10
Potassium, K mg 597 806 169 10
Sodium, Na mg 2 3 1 0
Zinc, Zn mg 6.45 8.71 1.83 0.11
Vitamins
Vitamin C, total ascorbic acid mg 0.8 1.1 0.2 0
Thiamin mg 0.364 0.491 0.103 0.006
Riboflavin mg 0.227 0.306 0.064 0.004
Niacin mg 4.387 5.922 1.244 0.075
Vitamin B-6 mg 0.094 0.127 0.027 0.002
Folate, DFE µg 34 46 10 1
Vitamin B-12 µg 0 0 0 0
Vitamin A, RAE µg 1 1 0 0
Vitamin A, IU IU 29 39 8 0
Vitamin E (alpha-tocopherol) mg 9.33 12.6 2.65 0.16
Vitamin D (D2 + D3) µg 0 0 0 0
Vitamin D IU 0 0 0 0
Source: United States Department of Agriculture (USDA), National Nutrient Database [28].

Forests 2017,8, 367 4 of 17
Table 2. Cont.
Nutrient Unit Value Per 100 g 1 Cup (135 g) 1 oz (167 Kernels)
or (28.35 g) 10 Nuts (1.7 g)
Vitamin K (phylloquinone) µg 53.9 72.8 15.3 0.9
Lipids
Fatty acids, total saturated g 4.899 6.614 1.389 0.083
Fatty acids, total monounsaturated g 18.764 25.331 5.32 0.319
Fatty acids, total polyunsaturated g 34.071 45.996 9.659 0.579
Cholesterol mg 0 0 0 0
Other
Caffeine mg 0 0 0 0
Source: United States Department of Agriculture (USDA), National Nutrient Database [28].
Pine nuts are beneficial for checking blood lipids and controlling coronary heart disease
(CHD) [
29
]. This is due to their containing only unsaturated fatty acids, whereas most other nuts also
have monounsaturated fatty acids, primarily oleic acid. However, pine kernels contain mostly linoleic
acid in the form of polyunsaturated fatty acids. Linoleic acid can be transformed into cellular mediators
that play an important role at the vessel level and improve blood coagulation [
30
]. P. koraensis Siebold
and Zucc and P. sibrica have the highest fat content—maximum 65–75%. Apart from their favorable
association with cardiovascular health, pine nuts are a rich source of other nutrients [
31
]. Table 3
presents a comparison of dietary values among species available in the world market. Interestingly,
pine nuts may also be used as natural appetite suppressants [19,32,33].
Table 3. Dietary values of several species of pine nuts in comparison with other commercially important nuts 1.
Type of Nut Carbohydrates (%) Fats (%) Protein (%)
P. pinea 7 48 34
P. gerardiana 23 51 14
P. edulis 18 62–71 14
P. sibrica 12 51–75 19
P. cembroides Zucc. 14 60 19
P. monophylla 54 23 10
P. koraiensis 12 65 18
P. sabiniana 9 56 28
1Percentages are approximate and based on shelled nuts. Source: Evaristo et al. [34]; Mutke et al. [27].
The chemical contents of pine nuts vary according to two main factors i.e., geographical range
and climate [
35
,
36
]. European pines (P. pinea) have specific fatty acids profiles that differ from Pakistani
pine nuts (P. gerardiana). This aspect has relevant interest concerning the issue of PNS as discussed in
the section on the results of the literature review.
3. Materials and Methods
The study is based on two connected analyses and related methodologies: A market survey
to provide robust evidence on the increased importance of the international pine nut trade,
and a literature review to highlight the underlying problems connected with the expansion of the nut
market—the phytosanitary aspects affecting pine forests and human health issues connected with
nut consumption.
EUROSTAT provided information for the elaboration of export and import data. The product
code (08029050 Pine “Pinus spp.” nuts, fresh or dried, whether shelled or not, or peeled) in the database
for international trade since 1988 (CN8 DS-016890) was used. However, we set 2006 as the base year
to avoid working with missing data prior to that year. From the EUROSTAT database average unit
values (
€
/Kg) and their annual variation have been elaborated for the five key EU trade players and

Forests 2017,8, 367 5 of 17
for the 28 EU member states as an aggregate (EU28). EUROSTAT trade data have been expressed as
extra-EU (for transactions with all countries outside of the EU) and intra-EU (all transactions occurring
within the EU).
For the literature review, we mainly used the Web of Science (WoS); the database was accessed
during January 2016–May 2017 and we did not limit our search to specific years, even if the main
publications considered are those of the last three decades.
4. Results
4.1. Production and Trade
Pine nuts are not commercially exported from Oceania [
17
]. They are mainly imported from
China, Spain, Italy and Turkey [
17
]. China and Pakistan have become main exporters over the past
decade to meet world demand [8,12].
The most popular edible variety is the European stone pine or umbrella pine (P. pinea), which has
been consumed by humans for more than 20 centuries [
26
,
37
]. Today, the Ligurian pesto from Italy has
pine nuts as an ingredient [38].
In recent years, market growth has been observed particularly in the US, becoming a 100 million
US$ market there [
10
,
29
]. The demand for pine nuts by consumers in the US has increased for the
last 10 years [
18
]. This trend might be explained by a recent Irish study that gave evidence that nut
consumption can help in decreasing the risk of coronary heart disease (CHD) and sudden cardiac
arrest [
29
]. There has recently been a hike in pine nut prices as gourmet products [
10
]. For instance,
in The Netherlands, 100 g of pine nuts costs 4
€
[
10
] while in Finland it can cost up to 5–6
€
depending
on the retailer. Three species of pine kernels (P. gerardiana,P. koraiensis, and P. pinea) as described in
FAO [
16
] have been part of global trade for many years, whereas P. sibirica entered the international
market in 2002 [39].
Tracking pine nuts along the supply chain is of increasing importance. Cases where nut species
were erroneously labeled due to lack of origin information have frequently been reported. Moreover,
re-exports among countries hinder the traceability of product origin. It occurs quite often that a consumer
is not supplied with adequate and suitable information regarding geographical origin, or even the
species of imported pine nuts on a product label.
Data are not available on world production of pine nuts [
16
]. The species are quite difficult
to distinguish from one another. According to Mutke et al. [
27
], even EUROSTAT and the Codex
Alimentarius have not devised differentiation procedures for pine nut species. Also in the case of trade
analysis the lack of specific trade codes (e.g., 0802.90.50 code in EUROSTAT database for pine nuts
versus 0802.90 in the UN COMTRADE database) limits the tracing of a gourmet product like P. pinea
nuts that yields a wholesale price of 45,000 to 60,000 €/t in Europe.
T and opportunities for policy makers” [
40
]. The report clearly states that pine nuts could not
be included in the two main nut categories proposed (the first consisted of coconuts, Brazil nuts
and cashew nuts, while the second gathered all the others—hazelnuts, walnuts, chestnuts and
pistachios—excluding pine nuts). According to Vidale et al. [
40
], the main obstacle for the inclusion
of pine nuts in the analyses was the single code used for mixed commodities of chestnuts, pistachios
and pine nuts together (reference HS6 code of the Multipurpose International Product Nomenclature
developed by the World Customs Organization).
According to the global statistical review 2014–2015 published by the International Nut and Dried
Fruit Council Foundation [
15
], world pine nut production was estimated at 39,950 MT (kernel basis).
This was 86% higher than in 2004. The increase was due to the expansion of China’s production
capacity which had grown 10 times since 2004. Indeed, China was the principal producer in 2014.
The crop yielded 25,000 MT (62% of total production share). Korea DPR came next (5000 MT or
12% share), followed by Afghanistan (3100 MT or 8% share) and Pakistan (3000 MT or 7% share).
Russian Federation contributed 2500 MT (6% share) to the world market (Geisler 2016). At the end of

Forests 2017,8, 367 6 of 17
2013, pine nut exports totaled 14,000 MT, i.e., 1.5 times the quantity exported in 2008. These observations
seem to confirm the export recovery trend that started in 2009. China shipped 10,683 MT, 76% of total
pine nut exports making it the main exporter; 29% of these exports went to the US. Note that China
appeared in the U.S. Bureau of the Census as an exporting country of pine nuts for the first time in
1976 [41].
The price development in Figure 1was estimated as average real price (2006–2016) of imported
products to the EU. EU imports are dominated by five countries (which cover about 98% of the
extra-EU import market in all the years considered). Prices increased at a remarkable rate, having
doubled in the last 10 years.
Forests 2017, 8, 367 6 of 17
seem to confirm the export recovery trend that started in 2009. China shipped 10,683 MT, 76% of total
pine nut exports making it the main exporter; 29% of these exports went to the US. Note that China
appeared in the U.S. Bureau of the Census as an exporting country of pine nuts for the first time in
1976 [41].
The price development in Figure 1 was estimated as average real price (2006–2016) of imported
products to the EU. EU imports are dominated by five countries (which cover about 98% of the extra-
EU import market in all the years considered). Prices increased at a remarkable rate, having doubled
in the last 10 years.
Figure 1. Price development estimated as average current prices of products imported to the EU
(2006–2016).
It is evident that unit values fluctuate sharply. Unlike in Italy and Spain, unit prices did not
dramatically shift in France, Germany and Great Britain. In fact, the exponential trend line increases
gradually over a number of years. This is an indication that trade is developing positively in terms of
demand for pine nuts in all 28 EU member states.
We have found some interesting research findings [1] concerning retailers of pine nuts all around
the world. A full list of countries and retailers that sold problematic pine nuts is represented in tabular
form (supplementary information). It is not the intention to ruin the reputations of the retailers nor
to suggest that buyers boycott them. It is just to give an idea that development of pine nut syndrome
to such a global extent is a serious issue. The names of pine species are usually missing from the
packet, which makes it almost impossible to trace their botanical origin [12]. Table 4 presents the total
number of PNS cases reported in 2011. It indicates that Australia, Canada, England, the Netherlands,
and the USA were the top five countries for the problem out of the 22 countries surveyed in the study.
Table 4. Summary of pine nut syndrome (PNS) cases reported during 2011.
Countries Number of Cases Reported Reported Cases (%)
Australia 15 4
Belgium 4 1
Canada 20 5
Czech Republic 1 0
Denmark 7 2
England 44 11
Finland 1 0
y= 750.33e0.0894x
0.0
500.0
1000.0
1500.0
2000.0
2500.0
2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016
Unit value (€/100 Kg)
DEU ESP FRA GBR ITA EU28 Expon. (EU28)
Figure 1.
Price development estimated as average current prices of products imported to the EU
(2006–2016).
It is evident that unit values fluctuate sharply. Unlike in Italy and Spain, unit prices did not
dramatically shift in France, Germany and Great Britain. In fact, the exponential trend line increases
gradually over a number of years. This is an indication that trade is developing positively in terms of
demand for pine nuts in all 28 EU member states.
We have found some interesting research findings [
1
] concerning retailers of pine nuts all around
the world. A full list of countries and retailers that sold problematic pine nuts is represented in tabular
form (supplementary information). It is not the intention to ruin the reputations of the retailers nor to
suggest that buyers boycott them. It is just to give an idea that development of pine nut syndrome to
such a global extent is a serious issue. The names of pine species are usually missing from the packet,
which makes it almost impossible to trace their botanical origin [
12
]. Table 4presents the total number
of PNS cases reported in 2011. It indicates that Australia, Canada, England, the Netherlands, and the
USA were the top five countries for the problem out of the 22 countries surveyed in the study.

Forests 2017,8, 367 7 of 17
Table 4. Summary of pine nut syndrome (PNS) cases reported during 2011.
Countries Number of Cases Reported Reported Cases (%)
Australia 15 4
Belgium 4 1
Canada 20 5
Czech Republic 1 0
Denmark 7 2
England 44 11
Finland 1 0
Germany 3 1
Hungary 1 0
Iceland 1 0
Ireland 3 1
Malta 1 0
Netherlands 51 13
New Zealand 4 1
Norway 3 1
Poland 1 0
Scotland 2 1
Singapore 1 0
Slovenia 1 0
South Africa 4 1
Sweden 6 2
USA 221 56
Total 395 100
Source: own elaboration from Tan [1]. The number of cases above 3 (or 1%) are indicated in italics.
4.2. Current Main Issues Affecting Pine Nuts Production and Trade
4.2.1. Pine Nut Syndrome
In 2001, Mostin first introduced the term ‘Pine Nut Syndrome’ (PNS) in the literature as a taste
disturbance [
13
,
36
,
42
]. Pine nut syndrome is also known as pine mouth syndrome (PMS) or pine nut
mouth syndrome [
17
,
24
,
36
,
43
–
46
]. Kwegyir-Afful et al. [
47
] introduced the term ‘Pine Mouth Event’.
Medically, it is known as dysgeusia, metallogeusia or cacogeusia [10,43,46,48].
According to Hampton et al. [
48
], the initial symptom is a persistent metallic or bitter taste starting
within hours to the first two days after eating pine nuts and can last for up to 14 days. In exceptional
cases, the metal or acid taste could last for a maximum of 42 days [
48
]. These pine mouth events went
unnoticed by the scientific community until cases reported by pine nut consumers rose dramatically
between 2008 and 2012 [
27
,
42
]. Consequently, several studies tried to investigate the taste disturbance
due to ingestion of pine kernels.
Apart from health aspects, lipids in pine nuts are of special importance due to their use in
identification of species causing the syndrome. Senter et al. [
49
], in their gas-liquid chromatography-mass
spectrometry experiment, suggested that phenolic acids in pine nuts (1.37
µ
g g
−1
) are relatively
higher than in almonds (1.08
µ
g g
−1
), filberts (0.36
µ
g g
−1
) and black walnuts (0.51
µ
g g
−1
). Phenolic
compounds might be the potential reason for taste disturbance as these possess an astringent
quality [
49
,
50
]. Weise [
51
] stated that the pine mouth events can happen due to rancidity of lipids.
Destaillats et al. [
12
] negated association of PNS to the oxidative reactions [
36
] of lipids identified in
their gas liquid chromatography analyses. It was also shown by Destaillats et al. [
12
] that the total
composition of fatty acids in Chinese kernels (P. armandii) did not differ markedly from the other
pine species in their experiment. From these studies, Köbler et al. [
50
] inferred that the fatty acid
composition of pine nuts does not influence taste disturbance. Möller [
24
] proposed that PNS may be
due to an elevated level of bile juice, which is produced as a result of bioactive compounds in pine

Forests 2017,8, 367 8 of 17
nuts. The effect might be compounded by enterohepatic recirculation, which dramatically extends the
residence time of many chemicals or drugs in the digestive tract.
No toxin, fungus, pesticide component or heavy metal had been evaluated as a direct reason
for generating PNS [
36
]. To the best of our knowledge, none of the studies (Table 5) provided
a relevant single cause for PNS development, though reliable methods were used, such as gas liquid
chromatography [
12
], fatty acid analysis and DNA testing [
37
], and/or nuclear magnetic resonance
analysis [
50
] to identify pine nut species from the reference samples. Even the most extensive study
on PNS conducted in France by Flesch et al. [
45
], proved unhelpful in this regard. Flesch et al. [
45
]
suggested that the bitterness might be caused by an unknown toxin. The toxin seemed to them to
be heat resistant. PNS is more frequent in females than males. They also hypothesized that this taste
disturbance might be due to a polymorphism in the genetic expression of taste functions.
In addition to PNS, Hampton et al. [
48
] briefly introduced the term anaphylaxis. For further details
regarding anaphylactic reactions, Cabanillas and Novak [26] have reviewed the issue quite clearly.
Most of the research in forestry dealt with pine trees (e.g., mainly ecology, historical aspects,
and tree health issues) rather than pine nuts. P. armandii Franch was often presented in the literature as
the most notorious species connected to PNS. This species grows in and comes directly from China.
It is very important to understand the true value of forest products so that they are utilized
sustainably and, if necessary, protected for harnessing future benefits. Most of the studies found
during the course of the present review were associated to PNS. Fortunately, we found some literature
related to the economic valuation of this nutritious product.
Masiero et al. [
52
], grouped 21 countries of the Mediterranean region into four sub-regions.
This arbitrary grouping was done to better estimate values for a selected set of products including
wood and non-wood forest products. Secondary data sources such as national reports, the FAO forest
resource assessment report published in 2010, and seven additional papers were used to derive pine
nuts results [
52
] (pp. 4–10). The pine nuts considered by Masiero et al. [
52
] were limited to P. pinea.
The minimum and maximum economic values for the different product ranges of pine nuts were
estimated. The two alternative scenarios were developed from the International Nut and Dried Fruit
Council’s report (min scenario) and the Mutke et al. (max scenario) paper published in 2012. The values
estimated were 83.8 M
€
to 307.7 M
€
for producing 5295 tons to 18,992 tons of pine nuts. According to
Masiero et al. [
52
], FAO Forest Resource Assessment (2010) indicated a market value of 48.7 M
€
for
the production of 16,545 tons of shelled pine nuts. Lebanon and Tunisia were regarded as important
producers with respect to the minimum production scenario and Spain performed best when the
maximum production scenario was applied.
Unfortunately, the Masiero et al. [
52
] study does not provide a holistic picture of different pine
nut species. This is due to its specific focus on Mediterranean pine nuts. However, limitations due to
a lack of official statistics and informal market channels for pine nuts justify the study.
Another study by Mutke et al. [
27
] also addressed and emphasized the importance of
Mediterranean stone pines (P. pinea). A forest owner can obtain higher profits from pine nuts than
harvesting timber in the Mediterranean region. In contrast to timber harvesting, revenue can be collected
annually by selling pine kernels without waiting for the long pine rotations. In semi-arid sandy and/or
rocky Mediterranean areas, the mean annual production of cones ranges 100–1000 kg ha
−1
which
can potentially yield 4–40 kg shelled pine nuts. So, prices in the world market are high enough
(50–60 €kg−1) to return an average income of 200–2400 €ha−1.
A number of challenges along the European nuts’ supply chain were of special interest in the
paper by Mutke et al. [
27
]. It was noted that legal and commercial differentiation of those available on
the market was without clear declaration of origin and species but under the generic name ‘pine nuts’.
For instance, in Germany P. koraiensis (Chinese nut) and P. gerardiana (Pakistani nut) were sold under
the name Pinienkerne (general name for pine nuts in the German language). Similar issues were raised
by Ballin and Mikklesen [
42
], who found P. armandii packed together with many other pine nut species.

Forests 2017,8, 367 9 of 17
Table 5. Summary of PNS studies.
Technique Used Cases Reported Case Study Study Scope References
Polymerase chain reaction (PCR)
amplicon with principal
component analysis (PCA)
NA GC SA Ballin and Mikkelsen (2016) [42]
Used Taqman-based real time
PCR method NA Italy (SC) SA Garino et al. (2016) [38]
Summarized the anaphylactic
cases in the paper 45 cases GC RA Cabanillas and Novak (2015) [26]
Genetic profiling of pine nuts 501 cases USA (SC) SA Kwegyir-Afful et al. (2013) [47]
Gas chromatographic method 4 cases Denmark (SC) SA Ballin (2012) [53]
Diagnostic index (DI) method
and recently developed method
in their laboratory
? The USA (SC) SA Fardin-Kia et al. (2012) [37]
Descriptive analysis of cases 3111 cases France (SC) SA Flesch et al. (2011) [45]
NA 1 case The UK (SC) L Hampton et al. (2011) [46]
Genetic method 15 cases USA (SC) SA Handy et al. (2011) [18]
Non-targeted nuclear magnetic
resonance (NMR) spectroscopy
and chemometrics
? GC SA Köbler et al. (2011) [50]
Online survey form 107 cases The Netherlands (SC) GL Tan (2011) [1]
NA NA The USA (SC) GL FDA (2011) [54]
NA
99% cases without
referring to total
number
The UK (SC) GL UKFSA (2011) [55]
Chemical and
morphological analysis NA France (SC) GL ANSES (2010) [13]
Gas-liquid
chromatography analysis ? GC SA Destaillats et al. (2010) [12]
NA NA Switzerland (SC) L Picard and Landis (2010) [44]
Standardized questionnaires as
well as lab tests 800 cases France (SC) GL AFSSA (2009) [56]
NA ? Ireland (SC) GL FSAI (2009) [57]
Abbreviations used: GC = General case; GL = Grey; L = Letter to scientific journal; NA = Not applicable; SA =
Scientific article; SC = Specific case; RA = Review article; ? = unknown.
The Sandeman Seeds Company labelled the UK as originator of those packets. However, we know
that P. armandii nuts grow and come mainly from China. Mutke et al. [
27
] attributed confusion in
detecting geographical origin of pine nuts to the concept of economies of scale (efficiencies formed by
volume) rather than economies of scope (efficiencies formed by variety). This is due to a number of
reasons such as the small size of pine nuts, dependence on a single product and supply, and current
commercial and market structure. In our opinion, these issues most probably just happened due to
re-exporting and re-importing of pine kernels.
The advent of modern device technology (mobiles and computers), internet, social networks and
online news articles debating PNS have started to negatively affect trade and market development
of pine nuts [
27
]. Although the international collection of food standards ‘Codex Alimentarius’ has
categorized pine nuts in TN 0673 since 1993 [
8
], a clear system is still lacking for classifying the most
important commercial species of pine nuts.
In some parts of the world, pine trees are mainly intended to better meet local consumption [
8
].
However, pine nuts might cause problems out of their native region. For instance, pine nuts imported
in the US are the main cause of PNS establishment because of their mixed nature [
39
]. This is because
pine nuts are difficult to distinguish morphologically. P. gerardiana is very similar to P. pinea. Similarly,
P. sibirica resembles P. armandii. Ultimately, re-exports among several countries mask the traceability of
origin and quality of the product. This is especially true when foreign suppliers normally sort and grade
(from company A to C instead of B) pine kernels based on the number of pine nuts per 100 g. Business

Forests 2017,8, 367 10 of 17
as usual varies greatly based on seed sizes e.g., 650–750 nuts/100 g to 1500–1700 nuts/100 g [
58
]. This is
why when pine nuts are purchased from a local market, species and geographical origin information is
seldom on the packets.
As mentioned earlier, the number of reported cases of PNS started to increase in 2009. We have
identified the following reasons in both the scientific as well as grey literature that might be directly or
indirectly responsible. Contributing factors may be a combination of the following. (1) Pine nuts are
extensively consumed worldwide as an ingredient in different foods, in both raw and roasted form.
The growing popularity and introduction of pine nuts in dishes such as tarts, pesto and gourmet salads,
desserts, breads, cakes, candies, vegetarian and non-vegetarian dishes, chocolates in Europe might be
a contributing element [
10
,
12
,
17
–
19
,
26
,
37
,
38
,
53
]; (2) A rapid exchange of information by consumers via
internet and the print media allow people to easily recognize the developing symptoms of PNS [
17
];
(3) Introduction of newer (non-traditional) species of pine nuts onto the global markets [
17
] as a result
of competitive global trade.
The first two causes of PNS development might have given rise to the fact that many studies
on pine nuts started to be done from the clinical toxicology, food and agricultural point of view.
The third cause (i.e., global trade) was neglected as is evident from the dearth of studies. In our
opinion, worldwide trade and the growing popularity of pine nuts in the food industry is a good
opportunity for forest scientists, pathologists, and societal marketing researchers to take the initiative.
The starting questions could be; which species would be good alternatives to those we already have?
Which species are the most profitable? How can plantations be managed to obtain a bumper pine nuts
crop? Why do a few tree species cause PNS while others do not?
Having said this, we acknowledge the fact that forest sciences research (particularly for societal
marketing researchers and economists) on pine nuts might not be simple due to the lack of reliable
data or a databank, which would hinder a full exploration of the trade aspects and valuation of pine
nuts. However, it will be a challenge for forest pathologists and entomologists due to climate change
and the increase in global trade of pine nuts, which are the main drivers of adventive insects. Table 5
summarizes the studies linked to PNS and economic valuations.
4.2.2. Pathogens and Pests of Pine Nuts
The introduction of emerging infectious diseases (EIDs) into new areas has been associated
to climate change, human ecology, increased global trade and economic growth [
59
,
60
]. A recent
study attributed seven underlying drivers (alien pathogenic invasion, climate change, emergence of
aggressive species or strains, rise in hybridization of fungi, latent and cryptic pathogens, establishment
of novel links between pathogens and their vectors, adaptation of new crops and cultivation practices)
of EIDs [
61
]. Often more than one driver may cause a rise in the range of pathogens, insects and
ultimately infectious diseases.
An increasing number of connections between adventive insects (acting as vector) and local
fungi (acting as pathogen) occur in forest ecosystems [
62
,
63
]. According to Ghelardini et al. [
61
],
establishment of novel links between pathogens and their vectors, climate change, latent and cryptic
pathogens are a few of the important factors identified that cause tip-blight of pines, also called
dieback, due to Diplodia sapinea or D. pinea and its association with an adventive insect, Leptoglossus
occidentalis Heidemann. Figure 2shows the current presence of L. occidentalis in the world. There are
many cone and seed insects of pines mentioned in the literature. For example, Dioryctria mendacella
Staudinger, Ernobius parens Mulsant and Rey, Ernobius impressithorax Pic, Pissodes validirostris Sahlberg,
and L. occidentalis [
64
–
68
]. However, L. occidentalis is one of the most extensively studied insect vectors
on pine nuts.

Forests 2017,8, 367 11 of 17
Forests 2017, 8, 367 10 of 17
The first two causes of PNS development might have given rise to the fact that many studies on
pine nuts started to be done from the clinical toxicology, food and agricultural point of view. The
third cause (i.e., global trade) was neglected as is evident from the dearth of studies. In our opinion,
worldwide trade and the growing popularity of pine nuts in the food industry is a good opportunity
for forest scientists, pathologists, and societal marketing researchers to take the initiative. The starting
questions could be; which species would be good alternatives to those we already have? Which
species are the most profitable? How can plantations be managed to obtain a bumper pine nuts crop?
Why do a few tree species cause PNS while others do not?
Having said this, we acknowledge the fact that forest sciences research (particularly for societal
marketing researchers and economists) on pine nuts might not be simple due to the lack of reliable
data or a databank, which would hinder a full exploration of the trade aspects and valuation of pine
nuts. However, it will be a challenge for forest pathologists and entomologists due to climate change
and the increase in global trade of pine nuts, which are the main drivers of adventive insects. Table 5
summarizes the studies linked to PNS and economic valuations.
4.2.2. Pathogens and Pests of Pine Nuts
The introduction of emerging infectious diseases (EIDs) into new areas has been associated to
climate change, human ecology, increased global trade and economic growth [59,60]. A recent study
attributed seven underlying drivers (alien pathogenic invasion, climate change, emergence of
aggressive species or strains, rise in hybridization of fungi, latent and cryptic pathogens,
establishment of novel links between pathogens and their vectors, adaptation of new crops and
cultivation practices) of EIDs [61]. Often more than one driver may cause a rise in the range of
pathogens, insects and ultimately infectious diseases.
An increasing number of connections between adventive insects (acting as vector) and local
fungi (acting as pathogen) occur in forest ecosystems [62,63]. According to Ghelardini et al. [61],
establishment of novel links between pathogens and their vectors, climate change, latent and cryptic
pathogens are a few of the important factors identified that cause tip-blight of pines, also called
dieback, due to Diplodia sapinea or D. pinea and its association with an adventive insect, Leptoglossus
occidentalis Heidemann. Figure 2 shows the current presence of L. occidentalis in the world. There are
many cone and seed insects of pines mentioned in the literature. For example, Dioryctria mendacella
Staudinger, Ernobius parens Mulsant and Rey, Ernobius impressithorax Pic, Pissodes validirostris
Sahlberg, and L. occidentalis [64–68]. However, L. occidentalis is one of the most extensively studied
insect vectors on pine nuts.
Figure 2.
Current distribution of Leptoglossus occidentalis around the world (source: EPPO
http://www.eppo.int).
Figure 2.
Current distribution of Leptoglossus occidentalis around the world (source: EPPO http://www.
eppo.int).
D. sapinea is a widespread pathogenic fungus also known as Sphaeropsis sapinea or D. pinea.
D. sapinea is commonly found in Europe, South Africa and the US. It is damaging for pines both in
their natural range and in plantations [
69
–
71
]. D. sapinea is badly damaging the cones of stone pine
(P. pinea) in Italy [
72
]. In 2013, the first report of D. sapinea on Scots pine (Pinus sylvestris L.) and
Austrian pine (Pinus nigra (Lodd. ex Lindl.)Munro) came from Sweden [
73
]. The conidia of D. sapinea
need L. occidentalis for their lengthy and extensive dispersal, though primary dissemination occurs via
rain splashes and wind currents [74].
L. occidentalis (Hemiptera; Heteroptera; Coreidae) is an indigenous species of the US [
75
] and is
commonly known as leaf-footed conifer seed bug or western conifer seed bug (WCSB). WCSB feeds on
seed sap by sucking and weakens the seed or even makes it abort [76].
Among numerous introduced groups of organisms in Europe, arthropods represent nearly
94% [
77
]. WCSB is one of the insect species that was introduced into Europe roughly 20 years ago.
It has been documented that it feeds on nearly 14 American and European conifer species: Pinus spp.,
Calocedrus decurrens (Torr.) Florin, Pseudotsuga menziesii (Mirb.) Franco, Tsuga canadensis (L.) Carrière,
Cedrus spp., Abies spp. and Picea spp. [
78
,
79
] are some of the important ones. WCSB was observed for
the first time in western North America. After World War II, it started to spread eastwards in the US
and Canada [80–86]. It was recorded for the first time in Vicenza, Italy during autumn 1999 [75,87].
Soon after its discovery in Italy, WCSB started to expand to other parts of the European continent.
It can now be found in Slovenia, Croatia, Hungary, Switzerland, Austria, Germany, and Czech Republic
to the north, and France to the west [
88
]. In 2003, it was also independently recorded in Spain [
88
].
WCSB was also found for the first time in Japan in 2009 [
89
]. During 2010, it was reported in Denmark
and Norway [
90
]. WCSB was first recorded in Russia in 2010 (Rostov Province) and in Ukraine in 2011
(Crimea and Zaporizhia Province) as cited by Gapon [
91
]. It was also first reported in Greece during
2011. The insect was collected from central Evia, Attica and the north of Peloponnese. It was mainly
found on Pinus halepensis Miller [
92
]. Recently, some researchers confirmed the presence of WCSB in
four regions of Chile i.e., Atacama, Metropolitan, Maule, and Bío Bío territories [93].
In northern Italy, WCSB can complete two or three generations per year [
94
]. In autumn, adults seek
shelter for their overwintering activities [
78
]. The adults and nymphs feed on cones and can potentially
create significant economic losses in high-value seed orchards [
65
,
76
,
95
]. WCSB has also been thought
to deteriorate the production of pine nuts for human consumption in Italian stone pine (P. pinea) stands.
Pine nuts production is decreased by the activities of WCSB in Italy, resulting in lower income [
96
] for
forest owners. Furthermore, it is notorious for causing a nuisance and damage to plumbing materials

Forests 2017,8, 367 12 of 17
when adult aggregates invade residential buildings for overwintering [
84
,
86
,
97
]. This is why they are
also known as urban bugs.
It is pertinent to say that beetles are usually associated as vector to plant pathogens in forests,
however, this was the first time a true bug (L. occidentalis) was observed to play a possible role as vector
for D. sapinea in a natural forest ecosystem [
98
]. During 2012, Luchi et al. [
98
] conducted an experiment
to understand the fungus and disease outbreak mechanism. They found a correlation between the
adventive L. occidentalis and native D. sapinea (S. sapinea). Molecular analysis (real-time PCR) showed
that D. sapinea was present both on the bodies of L. occidentalis and on the symptomless P. pinea cones
that were the insect’s main food source. Moreover, both organisms share similar habitat conditions.
The conspicuous damage on pine trees may be explained by their co-habitation that prompts the
disease spread and great invasive potential [99].
The results of a research conducted by Bracalini et al. [
68
] at Maremma regional park in Italy also
suggested that the low cone production and high number of damaged seeds agree with an overall
decline of stone pine nut production in Tuscany (Italy). The authors claim that the findings have been
confirmed by the local nut producing companies [68].
A fungus-insect interaction usually profits both parties [
98
]. The fungus takes advantage of the
insect via its dispersal to other pines or other tree species while the insect profits because the fungus
may stimulate the plant to produce monoterpenes, which are responsible for entomophilic community
formation. Similarly, a study on P. tabuliformis (Chinese pine) reported that the fungus Leptographium
procerum (W.B. Kendr.) (syn. Verticicladiella procera) raised levels of monoterpene attracting the insect
Dendroctonus valens L. [100] which acts as vector of the fungus.
Depending on climatic and environmental conditions, D. sapinea may act as a latent pathogen
enhanced by climatic stress and able to cause a speedy death of currently expanding shoots [
101
].
The potential involvement of WCSB in vectoring the conidia of D. sapinea was verified by Tamburini et al. [
87
].
At present, D. sapinea and L. occidentalis are not listed as pests recommended for regulation of quarantine
pests by the European and Mediterranean Plant Protection Organization [102].
5. Discussion and Conclusions
Information and data related to pine nuts are very limited in the literature. Most of the research
is focused on phytosanitary problems affecting pines and the related nut production and on taste
disturbance caused by pine nuts, PNS syndrome. The two issues are interlinked by the supply chain
development: an increased demand for pine nuts has stimulated the development of international
trade: to satisfy this increasing demand some pine nut species that cause PNS have been introduced in
the market. Unfortunately, there is very limited work on the analysis of market development for these
NWFP, partly due to recent growing demand in the western world and its informal market nature in
some large producing countries. However, in this rapidly developing market a systematic organization,
production presentation, and trade information by some global statistical institutions (e.g., FAOSTAT
and UN COMTRADE), is required. In fact, we have found that pine nuts information in relation to
its production, export and import is present in some regional statistical sources such as EUROSTAT,
but this information is limited, with special emphasis on EU markets. There are inconsistencies of
declared annual production and export data due to different levels of aggregation of the nut category
or the use of generic names for the groups of various species.
As for any other food commodity affecting human health, there is a need to track pine nut species
along the supply chain to prevent the introduction of invasive fungal and insect species. Ultimately,
pine nut species need to be supported in terms of the management of pine forests that may have
a relevant role in the economy and cultural value (landscape) of many countries, such as P. pinea in
the Mediterranean region. Future research should focus more on the economic importance of this
product, linking the pathological and entomological aspects of forest management to the human health
aspects with the aim of consolidating a responsible supply chain organization. To increase the income
generation from pine nuts more studies should be performed on integrated management of WCSB

Forests 2017,8, 367 13 of 17
(L. occidentalis) and D. sapinea, in addition to D. mendacella,E. parens,E. impressithorax,P. validirostris.
Due to the billion-euro pine nuts industry all around world, legislative bodies should pay special
attention to quarantine control of the wood movements containing potential pathogens and pests of
pine nuts.
Supplementary Materials:
The following are available online at http://www.mdpi.com/1999-4907/8/10/367/s1,
Table S1.
Acknowledgments:
This study was supported by the European Commission Erasmus+ program. We would also
like to show our gratitude to the Faisal Nadeem (China Agricultural University), Juha Rikala (Lecturer, University
of Helsinki), M. Ayyoub Tanvir (Lecturer, University of Agriculture, Faisalabad) for sharing their pearls of wisdom
with us during the course of this research, and we thank “anonymous” reviewers for their insights.
Author Contributions:
H.U.M.A. wrote the entire manuscript. D.P. conceived and did data analysis. All authors
contributed equally.
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
Tan, G. The Great Pine Nut Mystery. Available online: https://pinenutsyndrome.wordpress.com/pine-nut-
species/ (accessed on 22 June 2016).
2.
Phillips, A.J.L.; Alves, A.; Abdollahzadeh, J.; Slippers, B.; Wingfield, M.J.; Groenewald, J.Z.; Crous, P.W.
The Botryosphaeriaceae: Genera and species known from culture. Stud. Mycol.
2013
,76, 51–167. [CrossRef]
[PubMed]
3.
Slippers, B.; Boissin, E.; Phillips, A.J.L.; Groenewald, J.Z.; Lombard, L.; Wingfield, M.J.; Postma, A.;
Burgess, T.; Crous, P.W. Phylogenetic lineages in the Botryosphaeriales: A systematic and evolutionary
framework. Stud. Mycol. 2013,76, 31–49. [CrossRef] [PubMed]
4.
Lanner, R.M. The Pinon Pine: A Natural and Cultural History; University of Nevada Press: Reno, NV, USA, 1981.
5.
Millar, C.I. Early evolution of pines. In Ecology and Biogeography of Pinus, 1st ed.; Richardson, D., Ed.;
Cambridge University Press: Cambridge, UK, 1998; pp. 69–91.
6. Keeley, J.E. Ecology and evolution of pine life histories. Ann. For. Sci. 2012,69, 445–453. [CrossRef]
7.
Price, R.A.; Liston, A.; Strauss, S.H. Phylogeny and systematics of pinus. In Ecology and Biogeography of Pinus;
Richardson, D.M., Ed.; Cambridge University Press: Cambridge, UK, 1998; pp. 49–68.
8.
Mutke, S.; Calama, R.; González-Martínez, S.C.; Montero, G.; Javier Gordo, F.; Bono, D.; Gil, L. 4 Mediterranean
stone pine: Botany and horticulture. Hortic. Rev. 2012,39, 153–201.
9.
Ciesla, W.M. Non-Wood Forest Products from Conifers; Food and Agriculture Organization of the United
Nations (FAO): Rome, Italy, 1998; pp. 1–124.
10.
Zonneveld, B. Pine nut syndrome: A simple test for genome size of 12 pine nut–producing trees links the
bitter aftertaste to nuts of P. armandii zucc. Ex endl. Plant Syst. Evol. 2011,297, 201–206. [CrossRef]
11.
Sathe, S.K.; Monaghan, E.K.; Kshirsagar, H.H.; Venkatachalam, M. Chemical composition of edible nut seeds
and its implications in human health. In Tree Nuts: Composition, Phytochemicals, and Health Effects; CRC Press:
Boca Raton, FL, USA, 2009; pp. 12–36.
12.
Destaillats, F.D.R.; Cruz-Hernandez, C.; Giuffrida, F.; Dionisi, F. Identification of the botanical origin of pine
nuts found in food products by gas–liquid chromatography analysis of fatty acid profile. J. Agric. Food Chem.
2010,58, 2082–2087. [CrossRef] [PubMed]
13.
Administración Nacional de la Seguridad Social. Opinion of the French Agency for Environmental and
Occupational Health and Safety Concerning the Implementation of an Experimental Protocol for the Analysis of Pine
Nuts; Request No. 2009-SA-0289; French Agency for Food, Environmental and Occupational Health and
Safety: Paris, France, 2010; pp. 1–5.
14.
Hong, D.-Y.; Blackmore, S. Plants of China: A Companion to the Flora of China; Cambridge University Press:
Cambridge, UK, 2015.
15.
International Nut and Dried Fruit. Global Statistical Review 2014–15; International Nut and Dried Fruit:
Tarragona, Spain, 2015; pp. 38–41.
16.
Food and Agriculture Organization. Seeds, fruits and cones. In Non-Wood Forest Products from Conifers;
Food and Agriculture Organization (FAO): Rome, Italy, 1995.

Forests 2017,8, 367 14 of 17
17.
New South Wales Food Authority (NSWFA). Pine Nuts and pine Mouth—Emerging Issues Paper; New South
Wales Food Authority: Sydney, Australia, 2012; p. 25.
18.
Handy, S.M.; Parks, M.B.; Deeds, J.R.; Liston, A.; de Jager, L.S.; Luccioli, S.; Kwegyir-Afful, E.; Fardin-Kia, A.R.;
Begley, T.H.; Rader, J.I. Use of the chloroplast gene ycf1 for the genetic differentiation of pine nuts obtained
from consumers experiencing dysgeusia. J. Agric. Food Chem. 2011,59, 10995–11002. [CrossRef] [PubMed]
19.
Yu, L.; Slavin, M. 17 Nutraceutical potential of pine nut. In Tree Nuts: Composition, Phytochemicals, and Health Effects;
CRC Press: Boca Raton, FL, USA, 2008; p. 285.
20.
Calama, R.; Montero, G. Cone and seed production from stone pine (Pinus pinea L.) stands in central range
(Spain). Eur. J. For. Res. 2007,126, 23–35. [CrossRef]
21.
Calama, R.; Gordo, F.J.; Mutke, S.; Montero, G. An empirical ecological-type model for predicting stone
pine (Pinus pinea L.) cone production in the Northern Plateau (Spain). For. Ecol. Manag.
2008
,255, 660–673.
[CrossRef]
22.
Ovando, P.; Campos, P.; Calama, R.; Montero, G. Landowner net benefit from stone pine (Pinus pinea L.)
afforestation of dry-land cereal fields in Valladolid, Spain. J. For. Econ. 2010,16, 83–100. [CrossRef]
23.
Alasalvar, C.; Shahidi, F. Tree Nuts: Composition, Phytochemicals, and Health Effects; CRC Press: Boca Raton, FL,
USA, 2008.
24.
Möller, G. The Curious case of the Epicurean nut (Online Exclusive). Food Technol.
2010
,64. Available
online: http://www.ift.org/food-technology/past-issues/2010/may/features/online-exclusive- pine-nuts.
aspx (accessed on 29 January 2017).
25.
Gray, J. Nuts and seeds. In Encyclopedia of Human Nutrition, 2nd ed.; Lindsay, A., Prentice, A., Eds.; Elsevier:
Amsterdam, The Netherlands, 2005; Volume 4, p. 383.
26.
Cabanillas, B.; Novak, N. Allergic reactions to pine nut: A review. J. Investig. Allergol. Clin. Immunol.
2015
,
25, 329–333. [PubMed]
27.
Mutke, S.; Pastor, A.; Picardo, A. Toward a Traceability of European Pine Nuts “from Forest to Fork”.
In Proceedings of the International Meeting on Mediterranean Stone Pine for Agroforestry, Valladolid, Spain,
17–19 November 2011; pp. 17–19.
28.
United States Department of Agriculture. National Nutrient Database For Standard Reference Release 28;
United States Department of Agriculture: Washington, DC, USA, 2016.
29.
Ryan, E.; Galvin, K.; O’connor, T.; Maguire, A.; O’brien, N. Fatty acid profile, tocopherol, squalene and
phytosterol content of brazil, pecan, pine, pistachio and cashew nuts. Int. J. Food Sci. Nutr.
2006
,57, 219–228.
[CrossRef] [PubMed]
30.
Ros, E.; Mataix, J. Fatty acid composition of nuts–implications for cardiovascular health. Br. J. Nutr.
2006
,96,
S29–S35. [CrossRef] [PubMed]
31.
Nergiz, C.; Dönmez, I. Chemical composition and nutritive value of Pinus pinea L. Seeds. Food Chem.
2004
,
86, 365–368. [CrossRef]
32.
Hughes, G.M.; Boyland, E.J.; Williams, N.J.; Mennen, L.; Scott, C.; Kirkham, T.C.; Harrold, J.A.; Keizer, H.G.;
Halford, J.C. The effect of Korean pine nut oil (pinnothin
™
) on food intake, feeding behaviour and appetite:
A double-blind placebo-controlled trial. Lipids Health Dis. 2008,7, 6. [CrossRef] [PubMed]
33.
PinnoThin. The New Breakthrough Appetite Suppressant. Available online: http://www.dairyreporter.com/
Product-innovations/PinnoThin-The-new-breakthrough-Appetite-Suppressant (accessed on 28 June 2016).
34.
Evaristo, I.; Batista, D.; Correia, I.; Correia, P.; Costa, R. Chemical profiling of portuguese Pinus pinea L. Nuts.
J. Sci. Food Agric. 2010,90, 1041–1049. [PubMed]
35.
Zadernowski, R.; Naczk, M.; Czaplicki, S. Chemical composition of Pinus sibirica nut oils. Eur. J. Lipid Sci.
Technol. 2009,111, 698–704. [CrossRef]
36. Mostin, M. Taste disturbances after pine nut ingestion. Eur. J. Emerg. Med. 2001,8, 76.
37.
Fardin-Kia, A.R.; Handy, S.M.; Rader, J.I. Characterization of pine nuts in the US market, including those
associated with “pine mouth”, by GC-FID. J. Agric. Food Chem. 2012,60, 2701–2711. [CrossRef] [PubMed]
38.
Garino, C.; de Paolis, A.; Coïsson, J.D.; Bianchi, D.M.; Decastelli, L.; Arlorio, M. Sensitive and specific
detection of pine nut (Pinus spp.) by real-time PCR in complex food products. Food Chem.
2016
,194, 980–985.
[CrossRef] [PubMed]
39.
Sharashkin, L.; Gold, M. Pine Nuts: Species, Products, Markets, and Potential for Us Production. In Northern
Nut Growers Association 95th Annual Report, Proceedings of the 95th Annual Meeting, Columbia, MO, USA,
16–19 August 2004; The NNGA Library: Notre Dame, IN, USA, 2004.

Forests 2017,8, 367 15 of 17
40.
Vidale, E.; Riccardo, D.R.; Lovric, M.; Pettenella, D. NWFP in the International Market: Current Situation and
Trends; University of Padova: Padova, Italy, 2016.
41.
Little, E.L., Jr. Pine nuts (Pinus) imported into the United States. Gen. Tech. Rep. RM (USA)
1993
,236,
26–28. Available online: http://agris.fao.org/agris-search/search.do?recordID=US9443136 (accessed on
17 January 2017).
42.
Ballin, N.Z.; Mikkelsen, K. Polymerase chain reaction and chemometrics detected several pinus species
including Pinus armandii involved in pine nut syndrome. Food Control 2016,64, 234–239. [CrossRef]
43.
Munk, M.-D. “Pine mouth” syndrome: Cacogeusia following ingestion of pine nuts (genus: Pinus).
An emerging problem? J. Med. Toxicol. 2010,6, 158–159. [CrossRef] [PubMed]
44.
Picard, F.; Landis, B.N. Pine nut-induced dysgeusia: An emerging problem. Am. J. Med.
2010
,123, e3.
[CrossRef] [PubMed]
45.
Flesch, F.; Rigaux-Barry, F.; Saviuc, P.; Garnier, R.; Daoudi, J.; Blanc, I.; Tellier, S.S.; Lasbeur, L. Dysgeusia
following consumption of pine nuts: More than 3000 cases in france. Clin. Toxicol.
2011
,49, 668–670.
[CrossRef] [PubMed]
46. Hampton, R.; Scully, C.; Ellison, S. Pine mouth. Br. Dent. J. 2011,210, 151. [CrossRef] [PubMed]
47.
Kwegyir-Afful, E.E.; DeJager, L.S.; Handy, S.M.; Wong, J.; Begley, T.H.; Luccioli, S. An investigational
report into the causes of pine mouth events in US consumers. Food Chem. Toxicol.
2013
,60, 181–187.
[CrossRef] [PubMed]
48.
Hampton, R.L.; Scully, C.; Gandhi, S.; Raber-Durlacher, J. Cacogeusia following pine nut ingestion: A six
patient case series. Br. J. Oral Maxillofac. Surg. 2013,51, e1–e3. [CrossRef] [PubMed]
49.
Senter, S.; Horvat, R.; Forbus, W. Comparative GLC-MS analysis of phenolic acids of selected tree nuts.
J. Food Sci. 1983,48, 798–799. [CrossRef]
50.
Köbler, H.; Monakhova, Y.B.; Kuballa, T.; Tschiersch, C.; Vancutsem, J.; Thielert, G.; Mohring, A.;
Lachenmeier, D.W. Nuclear magnetic resonance spectroscopy and chemometrics to identify pine nuts
that cause taste disturbance. J. Agric. Food Chem. 2011,59, 6877–6881. [CrossRef] [PubMed]
51.
Weise, E. Pine Mouth: Hard to Crack; Rare Syndrome Linked to Nuts. Available online: https://usatoday30.
usatoday.com/news/health/2010-03-16-Pinemouth16_ST_N.htm (accessed on 10 March 2017).
52.
Masiero, M.; Pettenella, D.; Secco, L. From failure to value: Economic valuation for a selected set of products
and services from mediterranean forests. For. Syst. 2016,25, e051. [CrossRef]
53.
Ballin, N.; Hoorfar, J. Investigating cases of taste disturbance caused by pine nuts in Denmark. In Case Studies
in Food Safety and Authenticity: Lessons from Real-Life Situations; Woodhead Publishing Series in Food Science,
Technology and Nutrition: Cambridge, UK, 2012; pp. 318–325.
54.
FDA. “Pine mouth” and Consumption of Pine Nuts. United States Food and Drug Administration. Food and
Drug Administration. Available online: http://www.fda.gov/Food/RecallsOutbreaksEmergencies/
SafetyAlertsAdvisories/ucm247099.htm (accessed on 2 May 2016).
55.
United Kingdom Food Safety Agency (UKFSA). Pine Nuts from China. UK Food Standards Agency. United
Kingdom Food Safety Agency. Available online: http://www.food.gov.uk/business-industry/imports/
banned_restricted/pine-nuts-china/ (accessed on 10 July 2016).
56.
Agence Française de SécuritéSanitaire des Aliments (AFSSA). Information Regarding Reports of Bitter Taste
Following Consumption of Pine Nuts; Request No. 2009-SA-0166; Agence Française de sécuritésanitaire des
aliments/French Agency for Food, Environmental and Occupational Health and Safety (AFSSA): Paris,
France, 2009; p. 3.
57.
Food Safety Authority of Ireland (FSAI). Reports of Bitter Aftertaste from Eating Pine Nuts. Food Safety
Authority of Ireland. Available online: http://www.fsai.ie/news_centre/food_alerts/Pine_nuts.html
(accessed on 29 July 2016).
58.
Pinenut. How to Buy Grade AA Pine Nuts. Category Background. Available online: http://pinenut.com/
blog/blog1.php?title=extended-post&more=1&c=1&tb=1&pb=1 (accessed on 23 April 2016).
59.
Oaks, S.C., Jr.; Shope, R.E.; Lederberg, J. Emerging Infections: Microbial Threats to Health in the United States;
National Academies Press: Washington, DC, USA, 1992.
60.
Walther, G.R.; Roques, A.; Hulme, P.E.; Sykes, M.T.; Pyšek, P.; Kühn, I.; Zobel, M.; Bacher, S.; Botta-Dukát, Z.;
Bugmann, H.; et al. Alien species in a warmer world: Risks and opportunities. Trends Ecol. Evol.
2009
,24,
686–693. [CrossRef] [PubMed]

Forests 2017,8, 367 16 of 17
61.
Ghelardini, L.; Pepori, A.L.; Luchi, N.; Capretti, P.; Santini, A. Drivers of emerging fungal diseases of forest
trees. For. Ecol. Manag. 2016,381, 235–246. [CrossRef]
62.
Kenis, M.; Auger-Rozenberg, M.-A.; Roques, A.; Timms, L.; Péré, C.; Cock, M.J.; Settele, J.; Augustin, S.;
Lopez-Vaamonde, C. Ecological effects of invasive alien insects. Biol. Invasions 2009,11, 21–45. [CrossRef]
63.
Turgeon, J.J.; Roques, A.; Groot, P.D. Insect fauna of coniferous seed cones: Diversity, host plant interactions,
and management. Ann. Rev. Entomol. 1994,39, 179–212. [CrossRef]
64. Innocenti, M.; Tiberi, R. Cone and seed pests of Pinus pinea L. in central Italy. Redia 2002,85, 21–28.
65.
Bates, S.L.; Lait, C.G.; Borden, J.H.; Kermode, A.R. Measuring the impact of Leptoglossus occidentalis
(Heteroptera: Coreidae) on seed production in lodgepole pine using an antibody-based assay. J. Econ.
Entomol. 2002,95, 770–777. [CrossRef] [PubMed]
66.
Zherikhin, V. Pattern of insect burial and conservation. In History of Insects; Springer Science and Business
Media: New York, NY, USA, 2002; pp. 17–63.
67.
Ganatsas, P.; Tsakaldimi, M.; Thanos, C. Seed and cone diversity and seed germination of Pinus pinea in
strofylia site of the natura 2000 network. Biodivers. Conserv. 2008,17, 2427–2439. [CrossRef]
68.
Bracalini, M.; Benedettelli, S.; Croci, F.; Terreni, P.; Tiberi, R.; Panzavolta, T. Cone and seed pests of Pinus pinea:
Assessment and characterization of damage. J. Econ. Entomol. 2013,106, 229–234. [CrossRef] [PubMed]
69.
Luchi, N.; Longa, O.; Danti, R.; Capretti, P.; Maresi, G. Diplodia sapinea: The main fungal species involved in
the colonization of pine shoots in Italy. For. Pathol. 2014,44, 372–381. [CrossRef]
70.
Stanosz, G.R.; Smith, D.R.; Guthmiller, M.A. Characterization of Sphaeropsis sapinea from the west central
United States by means of random amplified polymorphic DNA marker analysis. Plant Dis.
1996
,80,
1175–1178. [CrossRef]
71.
Swart, W.J.; Wingfield, M.J. Biology and control of Sphaeropsis sapinea on pinus species in South America.
Detail 1991,30, 40.
72.
Santini, A.; Pepori, A.; Ghelardini, L.; Capretti, P. Persistence of some pine pathogens in coarse woody debris
and cones in a Pinus pinea forest. For. Ecol. Manag. 2008,256, 502–506. [CrossRef]
73.
Oliva, J.; Boberg, J.; Stenlid, J. First report of Sphaeropsis sapinea on scots pine (Pinus sylvestris) and Austrian
pine (P. nigra) in Sweden. New Dis. Rep. 2013,27, 23. [CrossRef]
74.
Palmer, M.; McRoberts, R.; Nicholls, T. Sources of inoculum of Sphaeropsis sapinea in forest tree nurseries.
Phytopathology 1988,78, 831–835. [CrossRef]
75.
Bernardinelli, I.; Zandigiacomo, P. Leptoglossus occidentalis heidemann (Heteroptera: Coreidae): A conifer
seed bug recently found in Northern Italy. J. For. Sci. 2001,47, 56–58.
76.
Bates, S.L.; Borden, J.H. Life table for Leptoglossus occidentalis heidemann (Heteroptera: Coreidae) and
prediction of damage in lodgepole pine seed orchards. Agric. For. Entomol. 2005,7, 145–151. [CrossRef]
77.
Roques, A.; Rabitsch, W.; Rasplus, J.-Y.; Lopez-Vaamonde, C.; Nentwig, W.; Kenis, M. Alien terrestrial
invertebrates of Europe. In Handbook of Alien Species in Europe; Springer Science and Business Media:
Dordrecht, The Netherlands, 2009; Volume 3, pp. 63–79.
78.
Koerber, T.W. Leptoglossus occidentalis (Hemiptera: Coreidae), a newly discovered pest of coniferous seed.
Ann. Entomol. Soc. Am. 1963,56, 229–234. [CrossRef]
79.
Krugman, S.L.; Koerber, T.W. Effect of cone feeding by Leptoglossus occidentalis on ponderosa pine seed
development. For. Sci. 1969,15, 104–111.
80.
Schaffner, J.C. The occurrence of Theognis occidentalis in the midwestern united states (Heteroptera:
Coreidae). J. Kansas Entomol. Soc. 1967, 141–142.
81.
Cibrián-Tovar, D.; Ebel, B.; Yates, H., III; Mendez-Montiel, J. Cone and seed insects of the Mexican
conifers. Universidad Autonoma Chapingo Secretary of Agriculture and Hydraulic Resources, Mexico.
In General Technical Report
; Southeastern Forest Experiment Service, USDA Forest Service: Asheville, NC,
USA, 1986.
82.
McPherson, J.; Packauskas, R.; Taylor, S.; O’brien, M. Eastern range extension of Leptoglossus occidentalis with
a key to Leptoglossus species of America North of Mexico (Heteroptera: Coreidae). Great Lakes Entomol.
1990,23, 99–104.
83.
Marshall, S. A new Ontario record of a seed eating bug (Hemiptera: Coreidae) and other examples of the role
of regional insect collections in tracking changes to Ontario’s fauna. In Proceedings of the Entomological
Society of Ontario, Guelph, ON, Canada, 1 June 1991; pp. 109–111.

Forests 2017,8, 367 17 of 17
84.
Gall, W. Further eastern range extension and host records for Leptoglossus accidentalis (Heteroptera:
Coreidae): Well-documented disperasl of a household nuisance. Great Lakes Entomol. 1992,25, 159.
85.
Ridge-O’Connor, G. Distribution of the western conifer seed bug, Leptoglossus occidentalis heidemann
(Heteroptera: Coreidae) in connecticut and parasitism by a tachinid fly, Trichopoda pennipes (F.) (Diptera:
Tachinidae). P. Entomol. Soc. Wash. 2001,103, 364–366.
86.
Bates, S.L. Damage to common plumbing materials caused by overwintering Leptoglossus occidentalis
(Hemiptera: Coreidae). Can. Entomol. 2005,137, 492–496. [CrossRef]
87.
Tamburini, M.; Maresi, G.; Salvadori, C.; Battisti, A.; Zottele, F.; Pedrazzoli, F. Adaptation of the invasive
western conifer seed bug Leptoglossus occidentalis to Trentino, an alpine region (Italy). Bull. Insectol.
2012
,
65, 161–170.
88.
Lis, J.A.; Lis, B.; Gubernator, J. Will the invasive western conifer seed bug Leptoglossus occidentalis heidemann
(Hemiptera: Heteroptera: Coreidae) seize all of Europe. Zootaxa 2008,1740, 66–68.
89.
Ishikawa, T.; Kikuhara, Y. Leptoglossus occidentalis heidemann (Hemiptera: Coreidae), a presumable recent
invader to Japan. Jpn. J. Entomol. 2009,12, 115–116.
90.
Mjøs, A.; Nielsen, T.R.; Ødegaard, F. The western conifer seed bug (Leptoglossus occidentalis heidemann, 1910)
(Hemiptera: Coreidae) found in SW Norway. Nor. J. Entomol. 2010,57, 20–22.
91.
Gapon, D. First records of the western conifer seed bug Leptoglossus occidentalis heid. (Heteroptera: Coreidae)
from Russia and Ukraine, regularities in its distribution and possibilities of its range expansion in the
Palaearctic region. Entomol. Rev. 2013,93, 174–181. [CrossRef]
92.
Petrakis, P. First record of Leptoglossus occidentalis (Heteroptera: Coreidae) in Greece. Entomol. Hell.
2011
,
20, 83–93.
93.
Faúndez, E.I.; Rocca, J.R. La chinche de las coníferas occidental, leptoglossus occidentalis heidemann
(heteroptera: Coreidae) en chile; rápida expansión, posibles impactos y desafíos (The western conifer seed
bug, Leptoglossus occidentalis heidemann (Heteroptera: Coreidae) in Chile; fast expansion, potential impact
and challenges). Rev. Chil. Entomol. 2017,42, 25–27.
94.
Bernardinelli, I.; Rovato, M.; Zandigiacomo, P. Life history and laboratory rearing of Leptoglossus occidentalis.
In Proceedings of the IUFRO Working Party 7.03. 10 Methodology of Forest Insect and Disease Survey in
Central Europe (2006), Gmunden, Austria, 11–14 September 2006; pp. 11–14.
95.
Strong, W.B.; Bates, S.L.; Stoehr, M.U. Feeding by Leptoglossus occidentalis (Hemiptera: Coreidae) reduces
seed set in lodgepole pine (Pinaceae). Can. Entomol. 2001,133, 857–865. [CrossRef]
96.
Roversi, P.; Strong, W.; Caleca, V.; Maltese, M.; Sabbatini Peverieri, G.; Marianelli, L.; Marziali, L.; Strangi, A.
Introduction into Italy of gryon Pennsylvanicum (ashmead), an egg parasitoid of the alien invasive bug
Leptoglossus occidentalis heidemann. EPPO Bull. 2011,41, 72–75. [CrossRef]
97.
Blatt, S. An unusually large aggregation of the western conifer seed bug, Leptoglossus occidentalis (Hemiptera:
Coreidae), in a man-made structure. J. Entomol. Soc. Br. Columbia 1994,91, 71–72.
98.
Luchi, N.; Mancini, V.; Feducci, M.; Santini, A.; Capretti, P. Leptoglossus occidentalis and Diplodia pinea: A new
insect-fungus association in Mediterranean forests. For. Pathol. 2012,42, 246–251. [CrossRef]
99.
Barta, M. Biology and temperature requirements of the invasive seed bug Leptoglossus occidentalis
(Heteroptera: Coreidae) in Europe. J. Pest Sci. 2016,89, 31–44. [CrossRef]
100.
Lu, M.; Wingfield, M.J.; Gillette, N.E.; Mori, S.R.; Sun, J.H. Complex interactions among host pines and fungi
vectored by an invasive bark beetle. New Phytol. 2010,187, 859–866. [CrossRef] [PubMed]
101.
Stanosz, G.; Blodgett, J.; Smith, D.; Kruger, E. Water stress and Sphaeropsis sapinea as a latent pathogen of red
pine seedlings. New Phytol. 2001,149, 531–538. [CrossRef]
102.
European and Mediterranean Plant Protection Organization (EPPO). Eppo A1 and A2 Lists Of Pests
Recommended for Regulation as Quarantine Pests; European and Mediterranean Plant Protection Organization:
Paris, France, 2017.
©
2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).